Ecological shifts underlie parallels between ontogenetic and evolutionary allometries in parrotfishes
Creators: name: Neves, Mayara
name: Westneat, Mark
name: Zelditch, Miriam
name: Brandl, Simon
name: Hugi, April
name: Chan, Howan
name: Titus, Kara
name: Arnold, Kaleigh
name: Evans, Kory
Publisher: name: Zenodo
Year: 2024
Subjects: Labridae
coral reef
development
allometry
Evolution

description: During ontogeny, animals often undergo significant shape and size changes, coinciding with ecological shifts. This is evident in parrotfishes (Eupercaria: Labridae), which experience notable ecological shifts during development, transitioning from carnivorous diets as larvae and juveniles to herbivorous and omnivorous diets as adults, using robust beaks and skulls for feeding on coral skeletons and other hard substrates. These ontogenetic shifts mirror their evolutionary history, as parrotfishes are known to have evolved from carnivorous wrasse ancestors. Parallel shifts at ontogenetic and phylogenetic levels may have resulted in similar evolutionary and ontogenetic allometric trajectories within parrotfishes. To test this hypothesis, using micro-CT scanning and 3D geometric morphometrics, we analyze the effects of size on the skull shape of the striped parrotfish Scarus iseri and compare its ontogenetic allometry to the evolutionary allometries of 57 parrotfishes and 162 non-parrotfish wrasses. The young S. iseri have skull shapes resembling non-parrotfish wrasses and grow towards typical adult parrotfish forms as they mature. There was a significant relationship between size and skull shapes, and strong evidence for parallel ontogenetic and evolutionary slopes in parrotfishes. Our findings suggest that morphological changes associated with the ecological shift characterizing interspecific parrotfish evolution are conserved in their intraspecific ontogenies.
description: Funding provided by: Division of Biological InfrastructureROR ID: https://ror.org/04qn9mx93Award Number: 1701665
Funding provided by: Division of Environmental BiologyROR ID: https://ror.org/03g87he71Award Number: 1541547
Funding provided by: MarineGEO*Crossref Funder Registry ID: Award Number: (S.J.B., 2015-2017)
Funding provided by: University of ChicagoROR ID: https://ror.org/024mw5h28Award Number: 
Funding provided by: Committee on Evolutionary Biology Hinds Fund*Crossref Funder Registry ID: Award Number: 
Funding provided by: Division of Environmental BiologyROR ID: https://ror.org/03g87he71Award Number: 2210200
Funding provided by: Division of Environmental BiologyROR ID: https://ror.org/03g87he71Award Number: 2237278
Funding provided by: Division of Biological InfrastructureROR ID: https://ror.org/04qn9mx93Award Number: 1701714
description: To investigate growth allometry, we examined the ontogenetic series of S. iseri, encompassing 54 individuals with a total length ranging from 1.75 to 33.5 cm. 

For skull shape comparison analyses among S. iseri, other parrotfishes, and non-parrotfishes wrasses, our sample of adults comprises 336 individuals (160 adult parrotfishes and 176 adult non-parrotfish wrasses) from 217 labrid fishes (Table S1). From this dataset, we compared the evolutionary allometry of Scarines reef clade (57 species) to ontogenetic allometry of S. iseri. The ontogenetic series of S. iseri was obtained through sampling carried out in Belize in 2023 (IACUC protocols: UT Austin/AUP-2021-00064 and SERC/10-15-15-SJB; Collection permits: BF000005-16 and BF0042-22) with additional individuals from the Field Museum of Natural History (FMNH). The remaining species were obtained through several museums (Table S1).

We assessed the three-dimensional skull shape of each labrid species through micro-computed tomography (μCT) scans. Specimens were scanned at Rice University, the University of Texas Austin, the University of Minnesota, and the University of Washington Friday Harbor Labs in conjunction with the scanAllFishes and oVert initiatives. The scans were segmented in Amira v2.0.0 (Thermo Fisher Scientific, Waltham, MA) to isolate the skull while eliminating scales and debris. The isolated skulls were transformed into 3D meshes and imported into Checkpoint (Stratovan, Davis, CA). We followed the landmark scheme of [19,28], however, three additional landmarks detailing points along the pectoral girdle were incorporated [27]. The characterization of shape variation involved 200 3D points, 83 landmarks, and 117 semi-landmarks. These points comprehensively sampled the pharyngeal jaws, oral jaws, neurocranium, nasals, hyomandibula, operculum, hyoid apparatus, and pectoral girdle. All points were exclusively situated on the left side of the skull.

To accommodate for the rotation and translation inherent in highly kinetic articulating components of the fish skull), we initially aligned each dataset through Generalized Procrustes analysis (GPA) using the gpagen function. Subsequently, a local superimposition was conducted to standardize the positioning of diverse skull elements [38,39]. To analyze the shape evolution of individual bones, we partitioned our extensive skull shape dataset into smaller datasets for each bone, and the raw coordinates were individually superimposed.  In this context, size was quantified as centroid size (CS), which represents the square root of the summed squared distances of each landmark to the centroid. After the local superimposition, we computed the average shapes and centroid sizes for the adult specimens of each species. All geometric morphometric analyses were carried out using the geomorph package, version 4.0.4 [40] in R, version 4.3.2 [41].