# Sniffing out morphological convergence in the turbinal complex of myrmecophagous placentals

Mark Wright, Quentin Martinez, Sérgio Ferreira-cardoso, Renaud Lebrun, Benjamin Dubourguier, Frédéric Delsuc, Pierre-henri Fabre, Lionel Hautier

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Mark Wright, Quentin Martinez, Sérgio Ferreira-cardoso, Renaud Lebrun, Benjamin Dubourguier, et al.. Sniffing out morphological convergence in the turbinal complex of myrmecophagous placentals. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 2024, 10.1002/ar.25603. hal-04892941

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**Title:** Sniffing out morphological convergence in the turbinal complex of myrmecophagous placentals

**Authors:** Mark Wright<fnref n="1" />,<fnref n="2" />, Quentin Martinez<fnref n="1" />,<fnref n="3" />, Sérgio Ferreira-Cardoso<fnref n="1" />, Renaud Lebrun<fnref n="1" />, Benjamin Dubourguier<fnref n="1" />, Frédéric Delsuc<fnref n="1" />, Pierre-Henri Fabre<fnref n="1" />,<fnref n="4" />, and Lionel Hautier<fnref n="1" />,<fnref n="4" />

**Affiliations:**

**Correspondence:** markwright@g.harvard.edu; lionel.hautier@umontpellier.fr

<footnote n="1">¹ISEM, Univ Montpellier, CNRS, IRD, Montpellier, France</footnote>

<footnote n="2">²Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA</footnote>

<footnote n="3">³Staatliches Museum für Naturkunde Stuttgart DE-70191, Stuttgart, Germany</footnote>

<footnote n="4">⁴Mammal Section, Life Sciences, Vertebrate Division, The Natural History Museum, London, United Kingdom</footnote>
**Abstract**

The length of the snout in mammals has important evolutionary consequences for the functional systems housed within the rostrum. However, whether increased snout lengths lead to expanded olfactory performance has rarely been examined. Here, we investigate inner rostral function among 10 species of myrmecophagous (ant- and/or termite-eating) placental mammals and 10 closely related species. We use non-destructive CT scanning methods to characterize inner rostral function based on the underlying morphology of the turbinal bones in the nasal cavity. Three approaches were chosen to address this question, including the quantification of functional turbinal surface area, the quantification of functional turbinal three-dimensional complexity, and geometric morphometrics. By including non-model species from several different mammalian orders, we were able to extend the discussion surrounding turbinal homologies to comparisons across mammals. Our results show no increased olfactory function in all myrmecophagous species relative to their sister taxa, which suggests that there is no trade-off for increased olfactory capabilities in myrmecophagous species with elongated snouts.
We found no evidence of convergence in turbinal morphology among all five myrmecophagous lineages. However, we found evidence of morphological convergence in the turbinals between the giant armadillo and the aardvark, suggesting a more complex interplay between the evolution of turbinal morphology and ecological correlates. While myrmecophagy alone may not be a strong enough ecological signal to overcome phylogenetic and developmental constraints, we suggest that this might be the case at the intersection of this dietary specialization with a primarily underground lifestyle where odorants may be difficult to detect.

**Key words:** morphology; turbinals; convergence; comparative anatomy; myrmecophagy; complexity.
Introduction

Myrmecophagous (ant- and/or termite-eating) mammals are a classic example of convergent evolution (McGhee, 2011). They are found in five different placental orders: Cingulata (armadillos), Pilosa (anteaters), Tubulidentata (aardvarks), Pholidota (pangolins), and Carnivora (aardwolves) (Fig. 1). While many mammals consume ants and/or termites, myrmecophagous species are highly specialized, relying almost exclusively on these invertebrates as a food source (Redford, 1987). Their shared morphological features include elongated snouts with extensible tongues, reduced or absent dentition, and claws for digging into ant and termite mounds (Feldhamer et al., 2007). Additionally, they display convergent gut microbiota (Delsuc et al., 2014; Teullet et al., 2023) and very low metabolic rates compared to most other mammals (McNab, 1984). Olfaction is broadly used for prey detection across mammals (Stoddart, 1980), and myrmecophagous species are no exception – armadillos (De Melo & Nogueira, 2020), anteaters (Lubin & Montgomery, 1981), aardvarks (Melton, 1976), pangolins (Mohapatra & Panda, 2014), and aardwolves (Richardson & Levitan, 1994) have all been documented making food choices while exhibiting sniffing behaviors. Despite similar snout morphologies and sniffing behaviors during predation, the internal anatomy of the olfactory system has never been investigated in a comparative phylogenetic framework for myrmecophagous mammals.

The nasal cavity of mammals is arranged as a tripartite capsule consisting of three regions defined by their location along the lateral wall during fetal morphogenesis: the pars anterior, the pars intermedia, and the pars posterior (Maier, 1993; Maier & Ruf, 2014; Martinez, Courcelle, et al., 2023; Ruf, 2020; Smith & Rossie, 2008). In each of these regions, cartilaginous precursors ossify into bones called turbinals. In adults, turbinals range in morphology from small, thin plates of bone to interweaving, paper-thin filigreed scrolls (Hillenius, 1992; Martinez, Okrouhlík, et al., 2023; Rowe et al., 2005; Smith et al., 2021). While there is disagreement
regarding the specific terminology used to describe individual turbinals (see Macrini 2012; Ruf 2014; Wagner and Ruf 2019; Lundeen and Kirk 2019; Martinez, Amson, et al. 2023 for a deeper discussion), they can broadly be categorized into two distinct functional types (Green et al., 2012; Martinez, Amson, et al., 2023; Martinez et al., 2018, 2020; Martinez, Okrouhlík, et al., 2023; Valkenburgh et al., 2011; Wagner & Ruf, 2019). The more anterior turbinals, which are involved in respiratory function, are covered with non-sensory epithelium that filters, warms, and humidifies air before it reaches the lungs (Jackson & Schmidt-Nielsen, 1964; Schmidt-Nielsen et al., 1970; Yee et al., 2016). The more posterior turbinals, which are involved in olfactory function, are covered with sensory epithelium that binds odorants circulating the nasal cavity and communicates sensory information to the olfactory bulb for processing (Purves et al., 2001; Smith et al., 2011; Smith & Bonar, 2022; Yee et al., 2016). Due to this variation in turbinal function, different selective pressures may influence turbinal morphology throughout the nasal cavity.

Respiratory turbinals evolved mainly in response to thermoregulatory demands (Schmidt-Nielsen et al., 1970). Because water conducts heat away from the body more quickly than air, transitions to more aquatic lifestyles require greater thermoregulatory control (Martinez, Amson, et al., 2023; Martinez et al., 2020; Martinez, Okrouhlík, et al., 2023; Valkenburgh et al., 2011). Aquatic mammals have long been described as having massively complex respiratory turbinals (Mason et al., 2020; Negus, 1956), and recent research in carnivorans (Valkenburgh et al., 2011) and more broadly across different mammal clades (Martinez et al., 2020; Martinez, Okrouhlík, et al., 2023) has confirmed significantly increased respiratory turbinal surface area in aquatic and amphibious mammals, which may correspond to greater capacity for respiratory function. A similar effect might be expected across a latitudinal gradient, but published results to date are less straightforward. A study comparing 20 caniform carnivoran species found no significant differences in respiratory turbinal size associated with latitude (Green et al., 2012).
However, comparisons of three individual sister taxa within the same study showed greater total turbinal surface area (both respiratory and olfactory turbinals) and chamber volume in Arctic species compared to more temperate ones, demonstrating the complex interplay of the many factors that influence turbinal morphology. Diet is an example of a factor that interacts with the environment in complex ways in terms of how it influences turbinal morphology. Olfactory turbinals are known to be associated with prey detection and are therefore influenced directly by diet. Large terrestrial carnivores that forage in widely dispersed habitats have expanded olfactory turbinal surface areas, which may help in the detection of odors over large distances or at low concentrations (Green et al., 2012; Martinez, Amson, et al., 2023; Martinez, Courcelle, et al., 2023; Pihlström et al., 2005; Valkenburgh et al., 2011). Aquatic mammals that forage underwater instead have a reduced olfactory turbinal surface area, which likely reflects a reduced reliance on olfaction to find prey in aquatic environments (Martinez, Courcelle, et al., 2023; Martinez et al., 2020; Valkenburgh et al., 2011). These studies demonstrate how both the environment and dietary specialization must be considered in testing the potential adaptations of turbinals.

In addition to distribution of sensory epithelium, the morphology of the inner nasal cavity has been demonstrated to influence airflow and potentially olfactory performance in dogs (Craven et al., 2007, 2010), cats (Pang et al., 2016; Wu et al., 2023), bats (Eiting et al., 2015), and strepsirrhine primates (Smith et al., 2019). Broadly, the effect of internal morphology is thought to slow down airflow to improve absorption of odorants in contact with olfactory mucosa, which may help in overall olfactory capability without modifying total surface area. Despite this functional explanation, comparative airflow dynamics in an ecological context are limited and suggest that selection for other demands on the snout, such as breathing and feeding, may override adaptive changes to airflow dynamics (Eiting et al., 2015). An alternative hypothesis could be that developmental changes that adaptively influence airflow dynamics are more
difficult to produce than simply increasing the overall surface area of turbinals, and thus it may
be a less common evolutionary path towards increased olfactory capability.

Here, we micro-CT scanned the skulls of ten myrmecophagous (anteaters, pangolins, aardvarks, pangolins, and aardwolves) and ten non-myrmecophagous (sister taxa) placental species (Fig. 1) to investigate whether the convergent evolution towards myrmecophagy included similar changes in turbinal morphology. We use multiple approaches for quantifying turbinals including direct surface area measurements, geometric morphometrics, and 3D complexity (Martinez et al., 2018). Myrmecophagous mammals need to detect highly specific odorants that may be concentrated deep within ant and termite mounds (Ocko et al., 2019). We hypothesize that these species will have well-developed olfactory turbinals to aid in prey detection. In addition to diet, turbinal morphology is constrained by morphological factors, and snout length in mammals has important evolutionary consequences for the functional systems housed within the rostrum. Feliform carnivorans have reduced snouts and display reduced olfactory turbinal surface areas (Valkenburgh et al., 2014), though computational fluid dynamics simulations suggest feliforms are still highly capable of efficient odorant detection (Wu et al., 2023), suggesting that constraints due to changes in overall snout morphology and size may alter how olfactory function is maintained throughout evolution. In contrast, whether a subsequent increase in snout length is associated with expanded olfactory turbinal surface area and complexity has rarely been properly investigated in other mammalian groups (see Martinez et al. 2018), and myrmecophagous species provide an ideal system to investigate this question.
# Materials and Methods

## Biological Samples

The materials sampled in this project belong to the collections at the Natural History Museum in London (NHMUK, London, United Kingdom), the Muséum National d'Histoire Naturelle (MNHN, Paris, France), the Museum of Vertebrate Zoology (MVZ, Berkeley, CA, United States), the American Museum of Natural History (AMNH, New York, United States), the Koninklijk Museum voor Midden-Afrika (KMMA, Tervuren, Belgium), the Institut Royal des Sciences Naturelles de Belgique (IRSNB, Bruxelles, Belgium), and the University of Montpellier (UM, Montpellier, France). The dataset is composed of 33 museum specimens (20 species) of myrmecophagous placentals (anteaters, giant armadillos, aardvarks, pangolins, and aardwolves) as well as closely related species (Table 1). For each of the following species, multiple individuals were analyzed to explore intraspecific variation in turbinal morphology: *Cyclopes didactylus* (n = 4), *Myrmecophaga tridactyla* (n = 2), *Tamandua tetradactyla* (n = 4), *Tamandua mexicana* (n = 4), *Phataginus tetradactyla* (n = 2), *Smutsia gigantea* (n = 2), and *Proteles cristatus* (n = 2). All collected specimens were adults except for one juvenile *T. tetradactyla* (NHMUK-75-1369) and one juvenile *S. gigantea* (MNHN-1913-113).

The phylogenetic relationships of the 20 focal species (Fig. 1) have been reconstructed based on complete mitochondrial genomes aligned using MAFFT v7 (Katoh & Standley, 2013) using Maximum Likelihood with RAxML v8 (Stamatakis, 2014) under the GTR+G model. The complete mitochondrial genome was unavailable for Tenrec ecaudatus, so only the 12S rRNA, Val-tRNA, 16S rRNA, and ND2 genes were used. Divergence dates were inferred using the RelTime method (Tamura et al., 2012) based on three fossil calibration constraints: Placentalia at 105 Million years ago (Mya), Xenarthra at 65 Mya, and Carnivora at 55 Mya (Puttick et al., 2016).
## Micro-Computed Tomography Scans

X-ray micro-computed tomography (µCT) scans were produced for each specimen using the SkyScan 1076 (ISEM, Montpellier) or the Nikon Metrology HMX ST 225 (NHMUK, London, United Kingdom). The voxel size for each scan was recorded in Table 1. Three-dimensional reconstructions were performed in AVIZO v. 9.4.0 software (Visualization Sciences Group, Burlington, MA, USA). For each specimen, turbinals in the left side of the nasal cavity were segmented by manually selecting and delimiting individual turbinals slice by slice (2-Dimensional selection) (Fig. 2). In one of the *T. tetradactyla* specimens, the left maxilloturbinal was broken, so the right maxilloturbinal was used instead. For each turbinal, three-dimensional surface meshes were generated to measure surface area, calculate three-dimensional complexity, and compare using geometric morphometrics, following Martinez et al. (2018). All 3D reconstructions were deposited in MorphoMuseum (Wright et al. 2024).

## Anatomical Terminology

As parts of the internal nasal skeleton, turbinals ossify from three chondrification centers: the pars anterior, the pars intermedia, and the pars posterior (Maier, 1993; Maier & Ruf, 2014; Martinez, Amson, et al., 2023; Ruf, 2020; Smith & Rossie, 2008). The maxilloturbinal is a medial attachment to the maxilla that develops from the ventral margin of the paries nasi (Macrini, 2012). The nasoturbinal and semicircular lamina (= lamina semicircularis) form a compound structure consisting of two components that develop from a ventral folding of the tectum and a lateral folding of the pars anterior, respectively (Macrini, 2012; Smith & Rossie, 2006) – in some adults, these two structures can be difficult to distinguish and appear as merged into one ossified element. The endoturbinals include turbinals in the ethmoturbinal recess that develop
as folds of the pars posterior, stretch to the midline of the nasal cavity, and coalesce rostroventrally to form the ethmoid plate, which, with the vomer, makes up the posterior transverse lamina (Macrini, 2012; Rowe et al., 2005). Finally, the ectoturbinals include any turbinal that attaches between the nasoturbinal and the first endoturbinal and develops as a fold of the pars intermedia (Allen, 1882; Macrini, 2012). In this study, all turbinals that ossify in the recessus frontoturbinalis are called frontoturbinals; all turbinals that ossify in the recessus ethmoturbinalis are called ethmoturbinals; interturbinals ossify in the spaces between already-ossified frontoturbinals and ethmoturbinals (Maier & Ruf, 2014; Paulli, 1900; Voit, 1909). When studying turbinal homologies, structures should ideally be classified using developmental series (Macrini et al., 2023). However, many extant vertebrate species, including all species investigated here, do not have growth series available to study. Pending future developmental studies, we consider the frontoturbinals to be equivalent to ectoturbinals, ethmoturbinals to be equivalent to endoturbinals, and interturbinals included in the former or latter depending on location.

The interturbinals may be incorrectly described in adult specimens as frontoturbinals or ethmoturbinals (Maier, 1993; Maier & Ruf, 2014; Martinez, Amson, et al., 2023; Rowe et al., 2005). These interturbinals are mostly found in the olfactory recess of the rostrum (but see also Martinez et al. 2020; Martinez, Amson, et al. 2023 for interturbinals elsewhere). Hypotheses on turbinal homology can be straightforward in mammals with relatively simple turbinals such as rodents, lagomorphs, bats and Eulipotyphla (e.g., Ruf 2014; 2020; Martinez et al. 2018; 2020; Martinez, Amson, et al. 2023; Ito et al. 2021; T. D. Smith and Bonar 2022). However, such hypotheses were more difficult to make in carnivorans (but see Wagner and Ruf 2019) and most of the myrmecophagous placental mammals studied here, which sometimes developed numerous fronto-, inter- and ethmoturbinals. In this study, the colors of the segmented turbinals aim to propose turbinal correspondence between species (see Martinez, Amson, et al. 2023).
The identified nasoturbinal (nt), maxilloturbinal (mt), semicircular lamina (sl), ethmoturbinal I (etl) as well as the interturbinal (it, in white, see Martinez, Amson, et al. 2023) are likely to be homologous between species. The frontoturbinals (fts) as well as the ethmoturbinals (ets, others than the etl) are colored according to their order from dorsal to ventral. Finally, we colored in pink other potential interturbinals (Figs. 1-7). From a functional perspective, a lack of direct homology between individual ethmoidal structures is not a limiting factor. We place turbinals into functional groups based on their location in the rostrum, following previous methodology from studies comparing turbinal function in adult specimens (Green et al., 2012; Martinez, Amson, et al., 2023; Martinez et al., 2018, 2020; Martinez, Okrouhlík, et al., 2023; Valkenburgh et al., 2011; Wagner & Ruf, 2019). Table 3 shows how the nomenclature used here for the purpose of making functional comparisons across our dataset compares to standard ontogenetic nomenclature in the literature.

Frontoturbinals and ethmoturbinals are considered to be serially homologous and are traditionally numbered from anterodorsal to posteroventral (Allen, 1882; Macrini, 2012, 2014; Paulli, 1900). Several of the species in this study contain turbinals that remain difficult to identify numerically using this terminology. For *Orycteropus afer* and *Priodontes maximus*, the majority of the frontoturbinals and ethmoturbinals interweave throughout each other, forming an intricate, entangled network of bone (Figs. 4C and 7B). For these species, numbering frontoturbinals from anterodorsal to posteroventral was not possible. The ethmoturbinals of these species are similarly indistinguishable except for ethmoturbinal I, which can be identified by its anterior protrusion alongside the maxilloturbinal. Because the remaining ethmoturbinals and frontoturbinals cannot be distinguished sequentially in all the species studied here, they are not numbered under assumptions of serial homology (Macrini, 2012; Macrini et al., 2023).

In the 3D renderings of the turbinals (Figs. 1-7), the colors match the proposed homology between species for the nasoturbinal, the maxilloturbinal, the ethmoturbinal I, the "main"
interturbinal, and the semicircular lamina. Both parts of the ethmoturbinal I (pars anterior and posterior) were similarly colored in red. The proposed interturbinals (excluding the "main" interturbinal) were colored in pink. These potential interturbinals were identified as interturbinals because of their relatively small size and because they generally do not project as far as the other turbinals (Martinez, Amson, et al., 2023). However, in adult mammals it is not possible to exclude the possibility that some of these "intertubinals" may be additional lamellae from other turbinals. We colored in white the "main" interturbinal (it) that is usually located between ethmoturbinal I (etl) and II (etll) (Martinez, Amson, et al. 2023), as it is likely homologous between species. In some species where the homology is not obvious, we considered the "main" interturbinal as the first relatively large interturbinal ventrally located next to the ethmoturbinal I. In species with numerous fronto- and ethmoturbinals, homologies with other species could not be proposed. Therefore, we colored the frontoturbinals alternating dark and light green and colored the ethmoturbinal (excluding the ethmoturbinal I) alternating yellow and orange.

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## Functional Turbinal Divisions

From the literature, it appears that the maxilloturbinal is primarily covered in respiratory mucosa across a wide taxonomic range while the frontoturbinals and most of the ethmoturbinals are primarily covered in olfactory epithelium (Green et al., 2012; Smith et al., 2011; Valkenburgh et al., 2011, 2014). However, histological stains of *Monodelphis* and *Microcebus* demonstrate that the nasoturbinal and ethmoturbinal I contain at least some degree of both respiratory and olfactory epithelium (Rowe et al., 2005; Smith et al., 2011).

In determining functional divisions for surface area and complexity comparisons, we compared three approaches: (1) the maxilloturbinal was classified as respiratory, while the rest of the turbinals (nasoturbinal, frontoturbinals, ethmoturbinals) were classified as olfactory
(following Green, 2012), (2) the maxilloturbinal and the anteroventral half of each the nasoturbinal and ethmoturbinal I were classified as respiratory, while the posterodorsal half of these structures and all remaining turbinals were classified as olfactory (following work from Rowe, 2005, and Smith, 2011), and (3) the maxilloturbinal was classified as respiratory, while the nasoturbinal and ethmoturbinal I were removed from consideration and the remaining turbinals were all classified as olfactory. In short, we found no significant differences between these approaches when comparing respiratory and olfactory surface area against body size proxies (AIC weights ranged from 0.02 to 0.56). For this reason, all models moving forward used the first method (1) for turbinal functional divisions.

## Geometric Morphometrics

For each specimen, 19 homologous 3D landmarks were placed on the reconstructed models of turbinals (Table 4, Fig. 2) using Avizo software (VSG Inc., Burlington, MA, USA). Generalized Procrustes analysis was performed on the coordinate data to obtain shape variables (Adams & Otárola, 2013; Goodall, 1991) using the “geomorph” package (Adams et al., 2022) in R version 3.5.0 (R Core Team, 2024). This method of generalized least-squares superimposition aligns all landmark configurations by optimally rotating, translating to the origin, and scaling to centroid size for each specimen. A multivariate analysis of variance (MANOVA) was performed on the principal component (PCA) scores that explained 90% of the variance to test for the effects of diet and phylogenetic order on turbinal shape using the “RRPP” package in R (Collyer & Adams, 2018). Additionally, Bloomberg’s K (n = 10,000 simulations) (Bloomberg et al., 2003) and Pagel’s lambda (Pagel, 1999) were calculated using the “phytools” package in R (Revell, 2012).
## Turbinal Complexity

We divided turbinal complexity into three qualitative types that exist along a spectrum of turbinal diversity: Type I - turbinals are considerably spaced and do not intertwine with other turbinals; Type II - turbinals are minimally spaced and may slightly intertwine with other turbinals; Type III - the turbinals are minimally spaced and heavily intertwine with other turbinals.

3D complexity measurements for each turbinal were performed in MorphoDig (Lebrun & Orliac, 2016). A convex hull, or the smallest convex set of points that contains the object in Euclidean space, was created for each turbinal. 3D complexity is a dimensionless metric and was defined as the area ratio between the surface area of the turbinal and the surface area of the encompassing convex hull (Martinez et al., 2018).

Functional divisions of turbinals for 3D complexity measurements are as follows: respiratory complex - the maxilloturbinal; and olfactory complex - the ethmoturbinals (except for ethmoturbinal I) and the frontoturbinals. The nasoturbinal and ethmoturbinal I were excluded here to avoid partitioning three-dimensional objects into uninformative subsets as they both contain at least some degree of each respiratory and olfactory epithelium (Martinez, Amson, et al., 2023; Martinez et al., 2020; Pang et al., 2016; Ruf, 2022; Smith et al., 2007, 2016; Yee et al., 2016). Respiratory turbinal complexity therefore is equivalent to the complexity of the maxilloturbinal, and olfactory turbinal complexity is calculated by taking the average complexity for the ethmoturbinals (not including ethmoturbinal I) and the frontoturbinals.

## Statistical Comparisons

The relationship between logged olfactory and respiratory turbinal surface area and complexity was investigated using the 'contMap' function from the 'phytools' package (Revell, 2024) in R (R Core Team, 2024). Analyses of variance (ANOVA's) were calculated to test for
differences in olfactory and respiratory turbinal surface area and complexity according to dietary specialization. Additionally, ANOVAs were performed to test for differences in the ratio between olfactory and respiratory turbinal surface area and complexity, respectively. To account for the species' shared evolutionary history, phylogenetic analyses of covariance (ANCOVA) were performed on total, respiratory, and olfactory turbinal surface area relative to two measures of body size (body mass and skull length) with dietary specialization defined as a factor in each model. The phylogenetic ANCOVAs were performed using the 'gls' function from the 'nlme' package, which allows the specified phylogeny to influence the correlation structure of the residual error (Pinheiro & Bates, 2000).

# Results

## Morphological Variation in Turbinals

Reconstructed models for each species are shown in Figs. 3-7 and, in more detail, in the Supplementary Materials. Within the nasal cavity of most species we observed, the general case for each turbinal is that the position tends to mirror the direction of the snout (through the text, we use the term "snout" to refer solely to the osteological portion of this region, while recognizing that the proper anatomical structure also includes soft tissue components such as cartilage). They are elongated rostrocaudally, exhibiting fractal-like, branching spirals along this axis. Occasionally, the ethmoturbinals and frontoturbinals among the species examined here are rotated about their mediolateral axis so that they are no longer parallel with the maxilloturbinal and nasoturbinal rostrocaudally. The semicircular lamina contains a wing-like lateral protrusion called the uncinate process. It forms the rostroventral border of the lateral recess in most of the species we observed. Considerable intraspecific variation exists in ethmoturbinal and frontoturbinal count (Table 5). The only exception to this variation is Cy.
*didactylus* (n = 4), consistently displaying four ethmoturbinals and two frontoturbinals (Table 5). Most turbinals exhibit Type I complexity, meaning they do not interweave and have considerable space between them. Type II complexity describes the maxilloturbinals and rostral portions of ethmoturbinal I in most of the Carnivora, while Type III complexity describes uniquely the ethmoturbinals and frontoturbinals of *P. maximus* and *O. afer*. In the following sections, each turbinal is described in more detail from a comparative perspective, highlighting the major features that differ among the species segmented in this study.

## Maxilloturbinal

In all specimens, the maxilloturbinal spans approximately from the rostral opening of the nasal cavity to the semicircular lamina, positioned ventrolaterally to the nasoturbinal. The maxilloturbinal is the most rostral turbinal in both sloth species (Fig. 3A-B), both *Dasypus* species (Fig. 4A-B), all five species of Carnivora and *M. culionensis* (Figs. 5, 6 and S1), *E. rozeti* (Fig. S1) *O. afer* and *T. ecaudatus* (Figs. 7 and S1). The opposite condition is observed in the two pangolin species *S. gigantea* and *P. tetradactyla*.

The maxilloturbinal is arbor-like in shape, except for two cases: (1) in *D. novemcinctus* (Fig. 4A) and *D. pilosus* (Fig. 4B), it is elongated rostrocaudally and pointed at the rostral end, and (2) in *B. tridactylus* (Fig. 3A) and *Ch. Didactylus* (Fig. 3B), it is elongated along its ventrodorsal axis. *B. tridactylus* (Fig. 3A) has a particularly unique maxilloturbinal, shaped triangularly along a rostrocaudal axis with the apex pointing ventrally and divided into two parts posteriorly. In *D. novemcinctus*, the maxilloturbinal is integrated to the skull posteriorly. The maxilloturbinal typically exhibits a single scroll but can also contain two or three branches (as in *P. maximus* and *O. afer*) or many bifurcating branches (as in *V. vulpes* and *A. lagopus*). Most often, the maxilloturbinal exhibits Type I complexity. Only *F. silvestris* (Fig. S1), *A. lagopus* (Fig. S1), and *V. vulpes* (Fig. 6A) exhibit Type II complexity, with the caudal part of the maxilloturbinal
intertwining with rostral portions of ethmoturbinal I in these specimens. The elongated snout of *M. tridactyla* (Fig. 4E) is reflected in its maxilloturbinal morphology, which is stretched and curved rostrocaudally. It is not the case in the largest pangolin species *S. gigantea*, which displays antero-posteriorly compressed maxilloturbinal.

The long axis of the maxilloturbinal is the same direction as the snout (rostrocaudal) except in a few species where the rostral end is elevated dorsally (Fig. 5A) and the caudal end is depressed ventrally (Figs 4B and 6C). The caudal-most attachment of the maxilloturbinal is either the floor of the nasal cavity or directly onto the lateral wall of the nasal cavity, and this caudal region of the bone sometimes exudes caudally on the ventral side of the semicircular lamina *in most of the species we observed*. In four of the five species of Carnivora (except *H. hyaena*), the caudal end of the maxilloturbinal does not reach all the way to the semicircular lamina (Figs. 5, 6 and S1). In these species, ethmoturbinal I fills much of the space left in this gap, and in *F. silvestris* (Fig. S1) the maxilloturbinal only occupies approximately one third of the total space in this gap. The maxilloturbinal of *S. gigantea* (Fig. 6C) connects posteriorly with the nasoturbinal and the semicircular lamina.

## Nasoturbinal

The nasoturbinal spans from the rostral opening of the nasal cavity to the semicircular lamina in all specimens. In all four species of anteaters (Fig. 3C, D, and E), *P. maximus* (Fig. 4C), and all three species of pangolins (Fig. 6B, C, and D), the nasoturbinal is the most rostral turbinal, extending beyond the rostral end of the maxilloturbinal. In *P. maximus*, it is noticeably larger in the ventrodorsal and mediolateral dimensions than most individuals in this study.

The nasoturbinal is arbor-like in shape, similar to the maxilloturbinal, but typically with a fewer number of spirals *in most of the species we observed*. In *M. tridactyla*, the nasoturbinal as
well as the uncinate process of the semicircular lamina elongate with the snout, the former
curving with the maxilloturbinal. The non-myrmecophagous armadillos *D. novemcinctus* (Fig.
4A) and *D. pilosus* (Fig. 4B) have rostrocaudally elongated nasoturbinals that are pointed at the
rostral end; the nasoturbinal extends posteriorly and transitions with the semicircular lamina in
the latter. On the other extreme, some species – as in *Cy. didactylus* (Fig. 3C) and *E. rozeti*
(Fig. S1) – contain only a very small process budding off the inner wall of the nasal cavity. The
nasoturbinal of *P. maximus* (Fig. 4C) particularly stands out as it contains an additional branch
that spans dorsolaterally around the maxilloturbinal. While continuous with the semicircular
lamina in most specimens, the caudal end of the nasoturbinal in *E. rozeti* (Supplementary
Plates) does not contain this ossification, and in *Ch. didactylus* (Fig. 3B) it is instead continuous
with ethmoturbinal.

Semicircular lamina

The semicircular lamina is an ethmoidal structure that is continuous and ossified with the
nasoturbinal in 19 of the 20 species in this study and shows the most variation in shape among
species examined here (Figs. 3-7, S1). In the adult *E. rozeti* (Fig. S1) as well as both juveniles
in this study (*S. gigantea* and *T. tetradactyla*), the nasoturbinal is completely separate from the
semicircular lamina. In most species, it contains a lateral wing-like expansion, or uncinate
process, which often curves caudoventrally around the rostral portion of the ethmoturbinals,
forming a border for the lateral recess. In some species (*B. tridactylus* and *F. silvestris*), the
uncinate process is reduced rostrocaudally (Figs. 3A and S1). The orientation of this lateral
expansion is almost directly lateral from the midline of the nasal septum but can also be rotated
so that the more lateral portions of this bone are ventral compared to its position along the
midline.
The uncinate process of *O. afer* (Figs. 7B and S1) gives rise to a particularly large concavity, which expands the volume of the anterior lateral recess at this location. However, the most extreme caudolateral extension of the uncinate process is in the three pangolin species, notably in *M. culionensis* where the uncinate process has a distinctly sickle shape (Figs. 6D and S1). Typically, the uncinate process terminates approximately near the anteriormost end of the ethmoturbinals, but in *M. culionensis*, this structure continues to extend caudally almost all the way to the cribriform plate.

The semicircular lamina is clearly divided into three parts (uncinate process, semicircular lamina intermedia, and semicircular lamina dorsal) in *M. tridactyla* (Figs. 3E and S1) and *D. novemcinctus* (Figs. 4A and S1). In *T. tetradactyla* (Fig. 3D), the semicircular lamina is fused with other lamina and the nasoturbinal, the limit between the latter being solely visible as the lateral recess opens. In *P. maximus* (Figs. 4C), the semicircular lamina anteriorly fuses with a process that originates from the horizontal lamina; the fusion forms a thick bone that is not here considered as the semicircular lamina (except for its dorsalmost part). In all five species of Carnivora (Figs. 5, 6A and S1), the caudal portion of the semicircular lamina beyond the uncinate process twists medially to attach to the nasal septum instead of proceeding straight to the cribriform plate as in most specimens. The semicircular lamina also contains a small turbinal-like process near its caudal-most end. This process can be a simple scroll or contain at least one spiral as in *H. hyaena* (Fig. S1).

## Ethmoturbinal I

Among the species examined here, the first ethmoturbinal is the largest and most rostral of the ethmoturbinals and sometimes extends quite far into the rostral portion of the nasal cavity. It is comprised of two distinct parts: the pars anterior, which varies considerably between individuals and accounts for the protrusion dorsal to the maxilloturbinal; and, the pars posterior,
which is similar to the rest of the ethmoturbinals in all of the species described here. The bulk of
the position of ethmoturbinal I is ventromedial to the nasoturbinal and frontoturbinals,
dorsomedial to the maxilloturbinal, and rostrodorsal to the remaining ethmoturbinals in most of
the species we observed.

The ethmoturbinal I in armadillos is highly dendritic (Fig. S1); its rostral portion is narrow
in both the ventrodorsal and mediolateral dimensions. In *D. pilosus*, the ventrolateral part of the
ethmoturbinal I forms the medial surface of a small sinus (Fig. S1). In *Ch. didactylus*, *M. tridactyla*, and both species of *Tamandua*, the rostral portion of ethmoturbinal I does not cover
the dorsal surface of the maxilloturbinal (Fig. S1). In the former, its anterior projection is
extremely small and forms a small sinus. *T. mexicana* (Fig. 3D) presents slight intraspecific
variation with two of the four individuals displaying an ethmoturbinal I that barely extends
rostrally enough to cover the caudal portion of the maxilloturbinal. This shorter protrusion is also
found in *Cy. Didactylus* (Fig. 3C), all three species of pangolins, and *B. tridactyla* (Figs. 3, 6, and
S1). In all species of armadillos (Figs. 4 and S1), *H. hyaena* (Figs. 5A and S1), *V. vulpes* (Figs.
6A and S1), *T. ecaudatus* (Figs. 7A and S1), *A. lagopus* and *E. rozeti* (Fig. S1), the rostral
portion extends until approximately the midpoint of the maxilloturbinal while blanketing its dorsal
surface. In *O. afer* (Figs. 7B and S1) and *F. silvestris*, (Fig. S1) this portion of ethmoturbinal I
extends nearly to the rostral end of the maxilloturbinal, and in *P. cristatus* (Figs. 5B and S1) it is
the most rostral turbinal found in the nasal cavity.

Similar to the previously discussed turbinals, ethmoturbinal I can be simple with a single
scroll, contain two or three branches, or contain many bifurcating branches. Most of the
specimens in this study exhibit Type I complexity for ethmoturbinal I. All five species of
Carnivora, however, exhibit Type II complexity in the rostral portion of ethmoturbinal I where it
intertwines with the maxilloturbinal. Although all armadillos display an ethmoturbinal I with Type
III complexity, it is most prominent in the giant armadillo, *P. maximus*, and the aardvark, *O. afer*.
In *Ch. didactylus*, ethmoturbinal I is in close contact with the semicircular lamina rostrally (Figs. 3B and S1). In several species, most prominently in *P. maximus* and *O. afer*, the caudal portion of ethmoturbinal I contains dozens of attachments to both the cribriform plate and the posterior transverse lamina. In most other specimens, the ethmoturbinals and frontoturbinals can be identified by having one unique root attachment to the cribriform plate and the posterior transverse lamina. However, in these specimens it is impossible to separate the caudal portion of ethmoturbinal I into smaller segments based on individual root attachment. Within the Carnivora, ethmoturbinal I and the ethmoturbinals immediately caudoventral to it are sometimes connected briefly before that the root attaches to the posterior transverse lamina. In *F. silvestris*, a distinct connection is lacking, with a second ethmoturbinal extending into the rostral nasal cavity above the maxilloturbinal.

In pangolins, the pars anterior and posterior of the ethmoturbinal I in *S. gigantea* (Fig 6C) are fused but may be distinguished from each other. This hypothesis needs to be clarified using ontogenetic data as investigated by Ito et al. (2023). In *P. tetradactyla* (Figs. 6B and S1), a small lamella is present between the pars anterior and the pars posterior of the etl. This lamella is connected to the horizontal lamina and the pars anterior of the etl, and likely corresponds to a part of the etl. In *M. culionensis* (Figs. 6C and S1), a turbinal is present between the pars anterior and the pars posterior of the etl; it is only connected to the horizontal lamina and does not extend medially as far as the other ethmoturbinals. In order to be consistent with our turbinal identification in other species, we colored it as an interturbinal. However, according to the pattern found in *Smutsia* and *Manis*, this turbinal may be a part of the etl. Alternatively this interturbinal (between the pars anterior and posterior of the etl) might correspond to the "main" interturbinal (it; in white in Fig. 6) and the subsequent ethmoturbinal will be the ethmoturbinal II and not the posterior pars of the ethmoturbinal I.
## Ethmoturbinals (excluding Ethmoturbinal I)

Most species examined here contain ethmoturbinals that spiral along an extended rostrocaudal length. They vary considerably in count between species and, to a lesser extent, within species (Table 5). Three of the smallest species in this study (*Cy. didactylus*, *T. ecaudatus*, and *E. rozeti*) as well as each species of Carnivora contain only a small number of ethmoturbinals (2-4). The ethmoturbinals in Carnivora are much larger than in the former three species despite being similar in count (Figs. 5, 6A, and S1). *B. tridactylus*, both species of *Tamandua*, and all three species of pangolins have a slightly larger number of ethmoturbinals (5-10). *D. pilosus*, *Ch. didactylus*, and *M. tridactyla* each contain a much larger number of ethmoturbinals (11-15), but only *P. maximus*, *O. afer*, and *D. novemcinctus* have more than 16 ethmoturbinals with *P. maximus* leading the way at 26 ethmoturbinals.

Most species in this study exhibit Type I complexity for the ethmoturbinals, but *P. maximus* and *O. afer* as well as to a lesser extent in the other three species of armadillos exhibit Type III complexity (Fig. S1). The ethmoturbinals of *P. maximus* and *O. afer* as well as to a lesser degree in the other three species of armadillos contain ethmoturbinals that form, in conjunction with the frontoturbinals, a curved hemisphere around the cribriform plate (Figs. 4, 7B, and S1).

As expected for an interturbinal, the "main" interturbinal identified did not develop large. One exception is *Dasypus pilosus* that developed a very large "main" interturbinal in comparison to *Dasypus novemcinctus* (Figs. 4 and S1). However, this is likely an artifact that connects the "main" interturbinal to the next ethmoturbinal. A CT-scan of higher resolution may help to resolve this.

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The number of additional interturbinals that slots between ethmoturbinals may vary from zero in various species (seven out of the twenty species, Table 5; Supplementary Plates) to 11 in *Priodontes maximus*. However, this attempt to distinguish between interturbinals and
ethmoturbinals is extremely difficult, especially in species with highly complex turbinals (e.g., in
armadillos and the aardvark) (Fig. 4, Fig. 7, and Supplementary Plates). As a result, the number
of interturbinals may be underestimated (e.g., in *Orycteropus afer*). An interesting intrageneric
variation is found in *Tamandua*, which presents a single interturbinal (in addition to the "main"
interturbinal) (Fig. 3 and Supplementary Plates). *Tamandua mexicana* displays an interturbinal
between the ethmoturbinal II and III while the interturbinal of *Tamandua tetradactyla* is the most
posterior turbinal, located next to the ethmoturbinal III (Fig. 3 and Supplementary Plates).

Frontoturbinals

Frontoturbinals, like ethmoturbinals, primarily resemble generic turbinal morphology (as described above) among species examined in this study but are typically smaller than the ethmoturbinals. In total count, both species of sloth, *Cy. didactylus*, *T. ecaudatus*, *E. rozeti*, both species of *Tamandua*, *F. silvestris*, *H. hyaena*, and *P. cristatus* have the fewest number of frontoturbinals (2-4) (Table 5). In *Cy. didactylus*, the two frontoturbinals may correspond to ft2 and ft3, since their root is lateral, while the first frontoturbinal generally has its root dorsally in other species with the turbinal projecting ventrally. However, with our current dataset of adult mammals, the homology remains unclear. Similar to the ethmoturbinals, the frontoturbinals of Carnivora are much larger relative to the others in this category (Figs. 5, 6A, and S1). All three species of pangolins as well as *V. vulpes* and *A. lagopus* have a slightly larger frontoturbinal count (5-10), while *D. pilosus* and *M. tridactyla* each have a considerably larger frontoturbinal count (11-15, Table 5). As with the ethmoturbinals, only *P. maximus*, *O. afer*, and *D. novemcinctus* have more than 16 frontoturbinals (Table 5). *O. afer* presents the largest number with 26 frontoturbinals (Table 5).

Similar to the ethmoturbinals, most of the species in this study exhibit Type I complexity
for the frontoturbinals (Fig. S1). The frontoturbinals of the pangolins are the most evident
example of Type I complexity, with large spaces between each individual turbinal (Fig. S1). In *P. maximus* and *O. afer* as well as to a lesser degree in the other three species of armadillos, the frontoturbinals, like the ethmoturbinals, exhibit Type III complexity (Fig. S1). In *P. maximus* and *O. afer* as well as the other three species of armadillos, the dorsal portion of the hemisphere around the cribriform plate is made up of frontoturbinals, but this hemisphere is less prominent in the latter three species of armadillos. The frontoturbinals of each of the five species of Carnivora are unique in that they extended dorsally into the frontal sinuses and are elongated rostrocaudally relative to the size of the nasal cavity (Figs. 5, 6A, and S1). Only in *Ch. didactylus* are the frontoturbinals also present in the frontal sinuses (Figs. 3B and S1), although they are not elongated. In *B. tridactylus*, the frontoturbinals are reduced in all dimensions and occupy little space (Figs. 3A and S1).

The number of additional interturbinals that slot between frontoturbinals may vary from zero (i.e., *Cy. didactylus*, *T. tetradactyla*, *T. mexicana*, *T. ecaudatus*, and *E. rozeti*) to ten (in *P. maximus*), but most species display a small number of them (Table 5). As for the ethmoturbinals, this number may also be underestimated in species with highly complex turbinals.

## Geometric Morphometrics

A principal component analysis (PCA) revealed that 90% of the variation in turbinal shape was explained by the first nine (out of 21) principal components (PCs). The first two PCs explained 49.5% of the total variance. In this morphospace (Fig. 8), myrmecophagous species only display slightly larger values along PC1 and PC2 compared to non-myrmecophagous species. In general, the myrmecophagous species display varied turbinal morphologies (Fig. 8). The pangolins sit in the middle of the morphospace, alongside *C. didactylus*. In contrast, the turbinals of the anteaters and the giant armadillo (*P. maximus*) occupy positive values of PC1 and PC2, corresponding to elongation of the snout and a slightly more caudal maxilloturbinal,
respectively. The turbinals of the aardvark (*O. afer*) clearly depart from this group showing the maximum positive values on PC2, which mainly express differences in height of the maxilloturbinal along the ventrodorsal axis. The turbinals of the southern aardwolf (*Proteles cristatus*) evolved towards the maximum values of PC2 and the minimum values of PC1, and are characterized by elongated and mediolaterally rotated maxilloturbinal. A multivariate analysis of variance (MANOVA) found that variation in turbinal shape was explained by both dietary specialization (p = 0.023) and taxonomic order (p = 0.001), though the latter explained most of the variance in the model (r² = 0.576 compared to 0.101 for diet). Further, the resulting morphospace indicates that separation by diet, though significant, is minimal (Fig. 8). Bloomberg's K (0.451) and Pagel's lambda (0.133) both suggest a departure from a Brownian motion explanation of evolution that could be in part explained by convergence, though neither test was statistically significant (p > 0.05).

## Turbinal Functional Divisions

A one-way analysis of variance (ANOVA) found no significant differences in turbinal surface area or complexity between myrmecophagous and non-myrmecophagous species based on dietary specialization (p > 0.05 for each model; Table 6). Phylogenetic analyses of covariance (ANCOVA) further demonstrated no effect of diet on relative total (p = 0.688), olfactory (p = 0.670, or respiratory (p = 0.808) turbinal surface area when taking into account the species' shared evolutionary history and adjusting for body mass (similar p-values were found when using skull length instead as a proxy for size) (Figure 10, Table 7). However, among myrmecophagous species, *P. maximus* and *O. afer* appear to represent outliers by showing a much higher olfactory turbinal surface area and 3D complexity (Figs. 9, 10, and S2).

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# Discussion

## Turbinal Homology

By including non-model species from several different mammalian orders, we were able to extend the discussion surrounding turbinal homologies to comparisons across mammals (Macrini 2012; Ruf 2014; Macrini et al. 2023; Martinez, Okrouhlík, et al. 2023; Martinez, Amson, et al. 2023). Under the hypothesis of serial homology, previous research has typically used a relative position numbering system to compare individual turbinals between different species (e.g., Macrini 2014). There are two major complications with this approach. First, in some cases it is not possible to number ethmoturbinals and frontoturbinals by relative position. The ethmoturbinals and frontoturbinals of *P. maximus*, *D. novemcinctus*, *D. pilosus*, and *O. afer* are interwoven with overlapping attachments to the cribriform plate and posterior transverse lamina. These turbinals are not positioned in an obvious sequential order for consistent numbering. Ordering the turbinals from anterodorsal to posteroventral in these species will yield a different sequence depending on whether counting is conducted closer to the posterior transverse lamina or closer to the cribriform plate. The second complication with this approach is that interturbinals, which ossify in the spaces between existing frontoturbinals or ethmoturbinals (Maier and Ruf 2014b; Ruf, 2014; Martinez et al. 2018, 2023c), are often not easily distinguished from surrounding turbinals in adult specimens. In some cases, such as non-model or fossil species, adult skulls are the only material available for study. As a result, serial homology is not a practical approach for interspecific comparisons and deep-time studies of turbinal evolution at the mammalian taxonomic scale.

Ridges on the inner surface of the nasal and maxillary bones have been identified in non-mammalian therapsids, indicating the presence of ossified turbinals prior to the origin of mammals (Hillenius 1992; Hillenius and Ruben 2004 but see Martinez, Okrouhlík, et al. 2023). A
current hypothesis for the number of ancestral ethmoturbinals in placentals includes four ethmoturbinals (Macrini, 2014; Moore, 1981). This count considers the pars anterior and posterior of the ethmoturbinal I (Fig. 2) as distinct turbinals. Previous research has identified four ethmoturbinals as well in fetal mouse lemurs, tenrecs, voles, and flying lemurs (Smith and Rossie, 2008). Macrini (2014) further suggested that the so-called endoturbinal III (not equivalent to the ethmoturbinal III here) in the marsupials *Caluromys philander* and *Monodelphis domestica* is an interturbinal and may have been lost in the placental lineage (Macrini, 2014). In general, factors influencing turbinal number appear to be clade-specific and might depend on the specific evolutionary constraints applying to each group (e.g., Martinez, Amson, et al. 2023). Our findings demonstrate considerable intraspecific and interspecific variation in the number of turbinals (Table 5), suggesting a greater plasticity than previously assumed. However, some trends are noticeable, ethmoturbinals are usually more numerous than frontoturbinals, with only a few exceptions (*M. tridactyla*, *O. afer*, *V. vulpes*, and *A. lagopus*). The relative number of ethmo- and frontoturbinals usually does not differ markedly, except that sloths have an unusually low number of frontoturbinals compared to ethmoturbinals.

We also observed that the number of interturbinals increases with the overall number of ethmo-
and frontoturbinals, and that this number is always higher in the most numerous type of
turbinals (either ethmo- or frontoturbinals). Pangolins consistently display a higher number of
ethmoturbinals compared to their carnivoran sister taxa (Table 5). The aardvark *O. afer* also
presents a much higher ethmoturbinal number when compared to its sister taxa (*T. ecaudatus*
and *E. rozeti*). These two cases could be intuitively linked to an adaptation to a
myrmecophagous diet, but we showed that the number of turbinals within Pilosa does not follow
a similar pattern (Table 5), with the giant anteater *M. tridactyla* being the only myrmecophagous
pilosan exhibiting larger ethmoturbinal and frontoturbinal numbers. Such differences might
suggest that differences in turbinal number might simply be taxon-specific and linked to spatial
and developmental constraints. Within a clade, we also observed that larger species tend to
present higher ethmoturbinal and frontoturbinal counts, suggesting that turbinal number might
also be related to body size (see Valkenburgh et al. 2014).

Turbinal Function

Mapping turbinal morphology to function has been an active area of research over the past two decades due to advancements in non-destructive scanning technologies (Joeckel et al., 2003; Rowe et al., 2005; Smith et al., 2004). Many studies have focused primarily on turbinal surface area as this metric is assumed to represent the total amount of epithelium lining each turbinal and may serve as a direct functional proxy (Valkenburgh et al. 2011; Green et al. 2012; Yee et al. 2016; Lundeen and Kirk 2019; Wagner and Ruf 2019; Martinez et al. 2018; Melin et al. 2022; Martinez et al. 2020; Martinez, Courcelle, et al. 2023; Martinez, Okrouhlík, et al. 2023, but see Martinez, Amson, et al. 2023). In this study, we grouped turbinals into morphological units (respiratory and olfactory complexes) and compared traits for each grouping among different species. Regarding functional turbinal classification, Green (2012) previously referred to the maxilloturbinal as respiratory and all other turbinals as olfactory. Ruf (2014) grouped the frontoturbinals and ethmoturbinals together as olfactory. Histological staining of *M. murinus* revealed 96% coverage of the nasoturbinal surface with olfactory epithelium (Smith et al., 2011). A histological stain of *M. domestica* showed that the apical surface of the nasoturbinal is primarily covered with olfactory epithelium, while the walls of the superior recess and maxillary sinus, the inferior surface of ethmoturbinal I, and the surface of the nasoturbinal facing away from the nasal lumen were lined with respiratory epithelium (Barrios et al., 2014; Harkema et al., 2006; Rowe et al., 2005). The rostral extension of ethmoturbinal I in felids has also been proposed to contain respiratory epithelium instead of olfactory epithelium to account for a shortened snout (Valkenburgh et al., 2014). Overall, the epithelial cover of the naso- and ethmoturbinal I greatly varies between species (e.g., T. D. Smith et al. 2004; T. D. Smith, Eiting,
and Rossie 2011; T. D. Smith and Rossie 2008; Yee et al. 2016; Martinez et al. 2020; Martinez,
Amson, et al. 2023; T. D. Smith, Eiting, and Bhatnagar 2012; Herbert et al. 2018) as well as a
dual function (e.g., T. D. Smith et al. 2007; 2016; Pang et al. 2016; Yee et al. 2016; Martinez et
al. 2020; Martinez, Amson, et al. 2023). Despite complex variation in the specific distribution of
epithelium on the nasoturbinal and ethmoturbinal I, we tested each hypothesis of turbinal
functional partitioning and found similar results, which suggests that different assumptions of
epithelial distribution do not have a significant effect on the comparison of olfactory performance
at the interspecific level. Further research should attempt to assess the distribution of epithelium
on the posterior transverse lamina, the mesethmoid, and the walls that bound and face into the
nasal cavity across a wide range of taxa, since these structures have also been identified from
histological stains as containing olfactory and respiratory epithelium (Barrios et al., 2014;
Macrini, 2014; Rowe et al., 2005; Smith et al., 2011).

While myrmecophagous and non-myrmecophagous species were discriminated in the
morphospace, our morphometric results primarily separated groups based on taxonomic order
rather than dietary specialization (Fig. 8). Comparison of functional turbinal surface area and
functional 3D complexity between groups revealed no significant separation between
myrmecophagous and non-myrmecophagous species (Table 6). Such an absence of difference
between the olfactory turbinals of myrmecophagous and non-myrmecophagous mammals does
not necessarily indicate that myrmecophagous mammals have similar olfactory capabilities than
non-myrmecophagous mammals. In fact, the establishment of a link between diet and the
surface area of the olfactory turbinals or their olfactory epithelium has been rarely tested
(Martinez, Amson, et al., 2023; Martinez et al., 2018; Melin et al., 2022; Valkenburgh et al.,
2014; Yohe et al., 2022), and the relation between olfactory turbinals, their genomics proxies, as
well as with olfactory capabilities has been questioned (Martinez, Amson, et al., 2023; Martinez,
Courcelle, et al., 2023). Increased size of the olfactory recess slows down airflow in the olfactory
region during both inspiration and expiration, allowing odorants to recirculate within the olfactory recess (Eiting et al., 2014). Turbinal morphology and complexity may also function to redirect airflow in the nasal cavity, as has been demonstrated in canids (Craven et al., 2007, 2010). Sniffing may also allow more air (and odor molecules) to enter the olfactory recess and circulate around and between turbinal bones (Rygg et al., 2017). A study investigating turbinal morphology among rodents identified increased 3D complexity of olfactory turbinals in species specialized for feeding primarily on underground earthworms, where higher olfactory sensitivity capabilities might be required (Martinez et al., 2018). More complex fractal-like turbinals in one region might cause differential circulation throughout the nasal cavity, which leads to adaptive responses without changes to the total surface area of a structure. If olfactory capabilities are primarily driven by the amount of epithelium, measures of surface area should capture most of the variation in performance. Instead, if redirecting airflow improves olfactory capabilities without increasing the amount of epithelium, surface area may not be as important as bone shape. In the latter scenario, 3D complexity may better approximate olfactory function with similar performance being potentially achievable through different morphologies. Performance tests should be conducted for each investigated species to properly characterize potential differences in olfactory function and link them to differences in olfactory shape and complexity.

Several myrmecophagous species are known to spend a significant amount of time underground (Nowak, 2018; Wilson & Mittermeier, 2009, 2011). In rodents, subterranean lifestyles increase hypoxia and hypercapnia, generating additional physiological stresses during ventilation not faced by their surface dwelling counterparts (Lacey & Patton, 2000). All myrmecophagous species are also characterized by a lower basal metabolic rate compared to most placental species (McNab, 1980). The maxilloturbinal is covered by a respiratory epithelium that functions to conserve heat (Hillenius, 1992; Schmidt-Nielsen et al., 1970). Reduced metabolic activity may require more respiratory epithelium to heat incoming air during
inspiration, corresponding to an enlarged maxilloturbinal. We found no significant differences in respiratory turbinal surface area or complexity between myrmecophagous and non-myrmecophagous species. Ratios of olfactory to respiratory surface area proved to be challenging to interpret here as higher ratios might result from the development of olfactory turbinals rather than a reduction of respiratory ones. In theory, lower demand for thermoregulatory capability would require less respiratory epithelium and might explain a reduction in maxilloturbinal size. Such reduction was particularly pronounced in the maxilloturbinal of *D. novemcinctus* and *D. pilosus*. Because armadillos live in burrows, they are subject to overheating and may have evolved carapaces with high minimum thermal conductance to adapt to the environment (McNab, 1980). A reduced need for thermoregulation may have played a role in the reduction in size of the maxilloturbinal in these armadillos, but the giant armadillo (*P. maximus*) also possesses a carapace and is not characterized by a reduced maxilloturbinal. Moreover, the role of the maxilloturbinal in thermal biology may not be as crucial as previously thought, with neither corrected basal metabolic rate nor body temperature being significantly correlated with the relative surface area of the maxilloturbinal at a mammalian scale (Martinez, Okrouhlík, et al., 2023). Here again, myrmecophagous species demonstrate that establishing a direct link between turbinal morphology and function can prove challenging, especially in understudied taxa.

## Morphological Convergence Among Myrmecophagous Mammals

The morphology of anteaters and pangolins is strikingly similar to the extent that taxonomists have previously suggested that they shared a direct common ancestor (Paulli, 1900; Wilson & Mittermeier, 2011). Molecular studies have shown that pangolins are instead more closely related to carnivorans, suggesting that similarities between anteater and pangolin morphology are the result of convergence (Delsuc et al., 2002; Meredith et al., 2011; Murphy et
al., 2001). Ferreira-Cardoso et al. (2019) demonstrated that convergent tooth loss resulted in divergent internal structures of the mandible of anteaters and pangolins despite the superficial resemblance of their masticatory apparatus (Ferreira-Cardoso et al., 2019). Here, we found that variation in turbinal morphology is explained more strongly by taxonomic order (p = 0.001, r² = 0.576) than by dietary specialization to myrmecophagy (p = 0.023, r² = 0.101), which reflects species distribution in the morphospace. In the morphospace, no PC separates anteaters and pangolins from the remaining species, and these two groups occupy minimally overlapping regions of the morphospace (Fig. 8). In particular, anteaters, except *Cy. didactylus*, occupy the maximum values along PC1 corresponding primarily to the elongated maxilloturbinals and nasoturbinals. Surface area and 3D complexity are unable to separate anteaters and pangolins from their sister taxa (Table 6). The main observable similarity among these species is an enlarged semicircular lamina (Figs. 3, 4, and S1). The semicircular lamina is generally covered by olfactory epithelium but because some variation exists among mammals, its exact function remains unclear (Martinez, Amson, et al., 2023; Smith & Bonar, 2022).

However, our detailed comparative descriptions suggest morphological convergence between the giant armadillo (*P. maximus*) and the aardvark (*O. afer*). The turbinals in these two species are complex, filigree scrolls that are interwoven and interlocked. They are relatively large in body size and dramatically different from the other species included in this study. *P. maximus* and *O. afer* display the highest number of combined ethmoturbinal and frontoturbinal counts, with 47 and 40, respectively (Table 5). However, they differ in the distribution of these turbinals, with *O. afer* showing an unusual higher number of frontoturbinals compared to ethmoturbinals. The caudal portion of ethmoturbinal I in these two species is also very complex in comparison to all other species examined, with many attachment sites to the cribriform plate and posterior transverse lamina. *O. afer* and *P. maximus* appeared similar in that their ethmoturbinals and frontoturbinals each exhibit exceptional complexity (Fig. 9). These two
species generally occupy regions of the morphospace with increased PC2 values,
corresponding to relatively constant ventrodorsal height of the turbinal complex from rostral to
caudal ends (e.g., contrast with *B. tridactylus*) (Fig. 8). However, there are many species with
high PC2 values, suggesting this axis of variation is not primarily associated with the unique
similarities between *O. afer* and *P. maximus* (Fig. 8). It is possible that generating morphospace
data using Type II landmarks, which were necessary here given the complex nature of turbinal
shape but are generally not as reliable indicators of homology as Type I landmarks, is not
capturing shape information that could distinguish these two species from the rest of the taxa.
Similarities between the surface area and complexity match with the significant correlation
between respiratory turbinal complexity and surface area found in rodents (Martinez et al., 2018;
Martinez, Okrouhlík, et al., 2023). The entire internal nasal system of these species may be
converging to a morphology different from other myrmecophagous mammals. These two
species are highly fossorial (Superina & Loughry, 2012; Taylor et al., 2002) and build burrows to
forage (Abba et al., 2005), although these ecological characteristics are also found in other
armadillos, which are not included in this study such as naked-tailed armadillos (*Cabassous
ssp.*) and fairy armadillos (*Chlamyphorus truncatus* and *Calyptophractus retusus*). However, the
burrows of *P. maximus* and *O. afer* are quite unique in their depth, so that they are considered
as burrowing ecosystem engineers (Desbiez & Kluyber, 2013; Louw et al., 2019). Furthermore,
these two species are known for spending much less time aboveground than other
myrmecophagous mammals (Nowak, 2018; Wilson & Mittermeier, 2011). In subterranean
rodents, odor discrimination has been demonstrated to be a method for identifying and
subsequently orienting digging towards edible plants (Heth et al., 2002; Heth & Todrank, 2007).
Increased size and complexity of olfactory structures are present in subterranean animals
ranging from cave-dwelling fish (Soares & Niemiller, 2013) to troglobitic beetles (Balart-García
et al., 2021). While the connection between modified structure and precise olfactory function
needs further research to elucidate, it is a reasonable explanation that reduced vision in dark
subterranean environments may be associated with increased reliance on olfactory or other
sensory capabilities across animals broadly. Although the structure and numbers of ethmo- and
frontoturbinals clearly diverged, the overall increased complexity and surface area of the
turbinals in these two species might relate to similarities in underground lifestyle, perhaps by
modifying turbinal morphology for odorants to circulate longer near the olfactory epithelium in
order to increase the chance of detection while underground. Maintaining efficient gas exchange
creates an additional physiological stress in hypoxic and hypercapnic conditions (Lacey &
Patton, 2000), which may explain why respiratory turbinals are more complex in addition to the
olfactory turbinals in these two fossorial and burrowing species.

As aardwolves have a very specific diet feeding almost exclusively on termites (Cooper &
Skinner, 1979; De Vries et al., 2011), we expected that their olfactory system might have shown
strong modifications for scent discrimination compared to closely related carnivorous hyaenids.
Among carnivorans, ethmoturbinal I extends furthest rostrally in the myrmecophagous southern
aardwolf (P. cristatus) (Fig. 5 and Supplementary Plates). Compared to its sister taxa, the
striped hyaena (H. hyaena), P. cristatus possesses extended ethmoturbinals and
frontoturbinals, which reflect the elongation of the snout found in other myrmecophagous
mammals (Fig. 5 and Supplementary Plates). Such elongation of the snout is also represented
in the morphospace (Fig. 8), with P. cristatus being set apart from other carnivorans. P. cristatus
has also a large ratio of olfactory to respiratory surface areas (Supplementary Figure S2).
However, it is difficult to draw clear conclusions from these observations. Indeed, olfaction is a
broad term that encompasses several different specific functions, such as detecting odorants at
low concentrations (sensitivity), discriminating between similar odors, or perceiving a wide range
of odorant molecules (Martinez, Courcelle, et al., 2023; Valkenburgh et al., 2014). Specific
olfactory functions may thus be advantageous in different ecological contexts. The aardwolf (P.
cristatus) scrapes dirt over its feces, and it has been hypothesized that this behavior helps to
mask the terpene scent of the termites, possibly to avoid olfactory confusion of feces with *Trinervitermes* feeding columns (Kruuk & Sands, 1972; Richardson, 1990). Such behavior could reflect an increased sensitivity to terpene odorants produced by this specific termite genus (Richardson & Levitan, 1994). With a lifestyle so focused on detecting the odorants produced by *Trinervitermes*, *P. cristatus* may be more effective at discriminating between odors than perceiving a wide range of odorant molecules, as might be necessary for the more generalist anteaters and pangolins.

## Conclusion

Surface area, 3D complexity metrics, and geometric morphometric results provide further evidence that the difference between turbinals in myrmecophagous and non-myrmecophagous species is minimal compared to the extent to which phylogeny shaped the evolution of these structures. Our comparative descriptions showed that the turbinal complexity in shape and numbers represents a potentially interesting source of morphological data for future phylogenetic systematics studies. Convergence in external traits such as snout length does not equate to convergence in the underlying internal skeleton structures. However, myrmecophagous species that spend a lot of time underground in their burrows (*O. afer* and *P. maximus*) have distinctly similar turbinal counts and complexity that may correspond to increased reliance on olfaction, though further research is needed to elucidate the precise relationship between structure and function in these species. The aardwolf (*P. cristatus*) also displays a modified olfactory system, which might relate to its extreme dietary specialization to detect the odorant of termites they exclusively feed on. In contrast, the anteaters and pangolins are more generalists and live above ground, and their turbinals may not be as constrained by odor sensitivity or discrimination. Olfaction is complex and consists of many underlying functions that are commonly described as a single sense. The nuance of describing differences in
olfaction should not be lost, and myrmecophagous mammals will provide an excellent system
for exploring these form-function relationships.

Acknowledgements

We express our gratitude to A-L Charruault (Institut des Sciences de l'Evolution in Montpellier),
Eleanor Hoeger (American Museum of Natural History), Géraldine Veron (Muséum National
d'Histoire Naturelle in Paris), and R. P. Miguez (Natural History Museum of London) for their
generous assistance in providing access to the mammal collections. The Nikon Metrology HMX
ST 225 was used to generate tomograms at NHMUK. MW was a student at the University of
Montpellier under the Erasmus Mundus Master Programme in Evolutionary Biology (MEME). At
ISE-M, scans were performed using the µ-CT facilities of the MRI platform member of the
national infrastructure France-Biolmaging. This research was mainly supported by a European
Research Council consolidator grant (ConvergeAnt; ERC-2015-CoG-683257), grants from the
French National Research Agency (CEBA: ANR-10-LABX-25-01; CEMEB: ANR-10-LABX-0004;
NUMEV: ANR-10-LABX-0020; Rhinograde: ANR-17-CE02-0005 RHINOGRAD 2017), and the
Alexander von Humboldt foundation (Q.M. FRA - 1222365 - HFST - P.). This research received
support from the Synthesys Project (www.synthesys.info) financed by the European Community
Research Infrastructure Action under the FP7 (GB-TAF-5606 and BE-TAF-5661). This is
publication ISEM-2024-214 of the Institut des Sciences de l'Evolution de Montpellier.
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**Table captions**

**Table 1**

List of species sampled in this study. Mass is from the MOM v4.1 global database of late Quaternary body mass (Smith 2003) except for *M. culionensis* which was taken from the Handbook of the Mammals of the World (Wilson 2011).

**Table 2**

Raw data used for analyses in this study. Mean values were taken for species with multiple individuals. Skull length was measured as the distance from the nasal bone to the superior notch of the foramen magnum. RSA = Respiratory Turbinal Surface Area; OSA = Olfactory Turbinal Surface Area; RTC = Respiratory Turbinal Complexity; OTC = Olfactory Turbinal Complexity

**Table 3**

Comparison of the functional nomenclature used in our study to the established ontogenetic nomenclature.
**Table 4**

Summary of the 19 homologous turbinal landmarks used in this study for geometric morphometric analysis.

**Table 5**

Number of ethmoturbinals and frontoturbinals for the species segmented in this study. The two juvenile specimens (one of each *T. tetradactyla* and *S. gigantea*) are not included here. Number of additional interturbinals (i.e., "main" interturbinal excluded) is presented in brackets.

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**Table 6**

Summary statistics from the analyses of variance for turbinal functional divisions. Two group tests are between myrmecophagous and non-myrmecophagous dietary specializations.

**Table 7**

Summary statistics from the phylogenetic analyses of covariance (ANCOVA) for turbinal division surface area relative to body mass and skull length with diet as a factor. Values correspond to Figure 10.
## Figure Captions

**Figure 1.** Phylogenetic framework for the 20 species considered in this study. Myrmecophagous species are indicated by red branches. The dataset includes five independent acquisitions of myrmecophagy (aardwolf, pangolins, aardvark, anteaters, giant armadillo). This chronogram has been generated through https://timetree.org/ (Kumar et al., 2022).

**Figure 2.** Lateral (A and B) and medial (C) perspectives of the segmented and reconstructed 3D surface meshes of *Tamandua tetradactyla*. The nasoturbinal and maxilloturbinal are colored in dark and light blue, respectively. The semicircular lamina is colored in grey. The ethmoturbinal I (pars anterior and posterior) is similarly colored in red. The "main" interturbinal is colored in white, the additional interturbinal is colored in pink. The frontoturbinals are colored in dark and light green, the ethmoturbinal (excluding the ethmoturbinal I) are colored in yellow and orange. Numbers correspond to homologous landmarks as defined in Table 5. *Abbreviations:* etl pa, ethmoturbinal I pars anterior; etl pp, ethmoturbinal I pars posterior; ets, ethmoturbinals; fts, frontoturbinals; it, "main" interturbinal; mt, maxilloturbinal; nt, nasoturbinal; pit, potential interturbinals; sl, semicircular lamina; up, uncinate process. Scale bar: 1cm.

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**Figure 3.** Lateral perspectives of the segmented and reconstructed 3D surface meshes of pilosan species investigated in this study. (A) *Bradypus tridactylus*; (B) *Choloepus didactylus*; (C) *Cyclopes didactylus*; (D) *Tamandua mexicana*; (E) *Myrmecophaga tridactyla*. More perspectives for each species are provided in the Supplementary Materials (S1). The nasoturbinal and maxilloturbinal are colored in dark and light blue, respectively. The semicircular lamina is colored in grey. The ethmoturbinal I (pars anterior and posterior) is similarly colored in red. The "main" interturbinal is colored in white, the additional interturbinal is

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colored in pink. The frontoturbinals are colored in dark and light green, the ethmoturbinal (excluding ethmoturbinal I) are colored in yellow and orange. Scale bar: 1cm.

**Figure 4.** Lateral perspectives of the segmented and reconstructed 3D surface meshes of cingulate species investigated in this study. (A) *Dasypus novemcinctus*; (B) *Dasypus pilosus*; (C) *Priodontes maximus*. More perspectives for each species are provided in the Supplementary Materials (S1). The nasoturbinal and maxilloturbinal are colored in dark and light blue, respectively. The semicircular lamina is colored in grey. The ethmoturbinal I (pars anterior and posterior) is similarly colored in red. The "main" interturbinal is colored in white, the additional interturbinals is colored in pink. The frontoturbinals are colored in dark and light green, the ethmoturbinal (excluding the ethmoturbinal I) are colored in yellow and orange. Scale bar: 1cm.

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**Figure 5.** Lateral perspectives of the segmented and reconstructed 3D surface meshes of the striped hyena (A, *Hyaena hyaena*) and the southern aardwolf (B, *Proteles cristatus*). More perspectives for each species are provided in the Supplementary Materials (S1). The nasoturbinal and maxilloturbinal are colored in dark and light blue, respectively. The semicircular lamina is colored in grey. The ethmoturbinal I (pars anterior and posterior) is similarly colored in red. The "main" interturbinal is colored in white, the additional interturbinals is colored in pink. The frontoturbinals are colored in dark and light green, the ethmoturbinal (excluding the ethmoturbinal I) are colored in yellow and orange. Scale bar: 1cm.

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**Figure 6.** Lateral perspectives of the segmented and reconstructed 3D surface meshes of the red fox (A, *Vulpes vulpes*) and three pangolin species: B, long-tailed pangolin (*Phataginus*
tricuspis); C, giant pangolin (Smutsia gigantea); and D, Philippine pangolin (Manis culionensis). More perspectives for each species are provided in the Supplementary Materials (S1). The nasoturbinal and maxilloturbinal are colored in dark and light blue, respectively. The semicircular lamina is colored in grey. The ethmoturbinal I (pars anterior and posterior) is similarly colored in red. The "main" interturbinal is colored in white, the additional interturbinals is colored in pink. The frontoturbinals are colored in dark and light green, the ethmoturbinal (excluding the ethmoturbinal I) are colored in yellow and orange. Scale bar: 1cm.

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**Figure 7.** Lateral perspectives of the segmented and reconstructed 3D surface meshes of two afrotherian species: A, tailless tenrec (Tenrec ecaudatus); and B, aardvark (Orycteropus afer). More perspectives for each species are provided in the Supplementary Materials (S1). The nasoturbinal and maxilloturbinal are colored in dark and light blue, respectively. The semicircular lamina is colored in grey. The ethmoturbinal I (pars anterior and posterior) is similarly colored in red. The "main" interturbinal is colored in white, the additional interturbinals is colored in pink. The frontoturbinals are colored in dark and light green, the ethmoturbinal (excluding the ethmoturbinal I) are colored in yellow and orange. Scale bar: 1cm.

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**Figure 8.** First two principal component axes comparing geometric morphometric results based off of 19 landmarks on the turbinal bones. The marker styles are separated into myrmecophagous (circle) and nonmyrmecophagous (diamond) species. Myrmecophagous mammals are in orange, non-myrmecophagous are in grey. Symbols represent the seven orders of mammals used in this study: squares, Cingulata; circles, Pilosa; star, Tubulidentata; crossed diamond, Afrosoricida; crossed square, Macroscelidea; small diamonds, Pholidota; triangles, Carnivora. Maximum and minimum extreme shapes are plotted along each PC axis representing lateral (left) and medial (right) perspectives, respectively.
**Figure 9.** Left, evolution of the surface area and complexity of olfactory (top) and respiratory (bottom) mapped onto a phylogeny including all studied taxa. Right, box plots of functional complexity (logarithm) ratio by dietary specialization (top, olfactory turbinals; bottom, respiratory turbinals. Colors correspond to the two dietary specialization groups (red: myrmecophagous; grey: non-myrmecophagous). More details for each mammalian order are provided in the Supplementary Materials (S2).

**Figure 10.** Phylogenetic analyses of covariance (ANCOVA) for turbinal division surface area relative to body mass and skull length with diet as a factor: (A-B) log10 total turbinal surface area; (C-D) log10 respiratory turbinal surface area; (E-F) log10 olfactory turbinal surface area; (A, C, E) log10 body mass (kg); and, (B, D, F) log10 skull length (mm). Colors correspond to the two dietary specialization groups (orange: myrmecophagous; grey: non-myrmecophagous).

**Supplementary data.**

S1. Plates of all individual species studied: A, lateral of the cranium and turbinals; B, medial view of the turbinals (mirror image); C, dorsal view of the turbinals; D, section through the maxillo- and nasoturbinals; E, section through the fronto- and ethmoturbinals.

S2. Box plots of the functional ratios of the logarithm of the surface area (A) and complexity (B) by dietary specialization, Colors correspond to the two dietary specialization groups (red: myrmecophagous; grey: non-myrmecophagous).
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<figure><img src="image_5.png" /><figcaption>B</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>C</figcaption></figure>

<figure><img src="image_7.png" /><figcaption>D</figcaption></figure>

<figure><img src="image_8.png" /><figcaption>E</figcaption></figure>

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A

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B

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C

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A

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B

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A

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B

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C

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D

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A

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B

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PC2: 19.1%

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PC1: 30.4%

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<figure><img src="image_26.png" /><figcaption>A</figcaption></figure>

<figure><img src="image_27.png" /><figcaption>Dietary Specialization</figcaption></figure>

<figure><img src="image_28.png" /><figcaption>B</figcaption></figure>

<figure><img src="image_29.png" /><figcaption>Dietary Specialization</figcaption></figure>
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