DOI: 10.5061/dryad.37pvmcvt0
title: The neoteny Goldilocks zone: The evolution of neoteny in Ambystoma

description: Neoteny is a developmental strategy wherein an organism reaches sexual
 maturity without associated adult characteristics. In salamanders, neoteny
 takes the form of individuals retaining aquatic larval characteristics
 such as external gills upon maturation. Mole salamanders (Ambystoma)
 occupy a wide range of habitats and areas across the North American
 continent and display examples of non-neotenic, facultatively neotenic,
 and obligate neotenic species, providing high variation for investigating
 the factors influencing the evolution of neoteny. Here, we use
 phylogenetic comparative methods to test existing hypotheses that neoteny
 is associated with elevational and latitudinal distribution,
 cave-associated isolation, and hybridisation-related polyploidy. We also
 test if neoteny influences the diversity of habitats a species can occupy
 since the restriction to aquatic life should constrain the availability of
 different niches. We find that neoteny tends to occur in a narrow
 latitudinal band between 20-30° North, with particularly narrow
 latitudinal ranges for obligate compared to facultative neotenic species
 (16-52° North). We also find that facultatively neotenic species occur at
 elevations more than twice as high as other species on average and that
 species with a higher frequency of neoteny typically have lower habitat
 diversity. Our results suggest that evolutionary transitions between
 non-neotenic and facultative neoteny states occur at relatively high and
 approximately equal rates. Moreover, we estimate that obligate neoteny
 cannot evolve directly from non-neotenic species (and vice versa), such
 that facultative neoteny acts as an evolutionary ‘stepping stone’ to and
 from obligate neoteny. However, our transition rate estimates suggest that
 obligate neoteny is lost &gt; 4 times faster than it evolves, partly
 explaining the rarity of obligate species. These results support the
 hypothesis that low latitudes favour the evolution of neoteny, presumably
 linked to more stable (aquatic) environments due to reduced seasonality,
 but once evolved it may constrain the diversity of habitats.
description: Maximum elevation data was taken from the IUCN Red List database
 (IUCN 2021) for all species except the
 following; <em>A. barbouri</em> (Micheletti
 and Storfer 2015), <em>A.bishopi, A. mabeei, A. maculatum,
 A. talpoideum, A. texanum,
 A. talpoideum, A.texanum</em> (observations from AmphibiaWeb 2021,
 checked for elevation
 on www.freemaptools.com/elevation-finder.htm), <em>A. californiense</em> (Lanoo 2005), <em>A. cingulatum,</em> (animaldiversity.org 2021), <em>A. jeffersonianum</em> (Thompson and Gates 1982), and <em>A. opacum</em> (Klemens 1993). Latitudinal data (northern and southern distributional limits) were collected using the species distributions from the IUCN Red List database (IUCN 2021). The number of habitats occupied by each species was estimated by counting the second-level habitat types (for example 1.4 Forest -Temperate) listed in the IUCN Red List (IUCN 2021) according to their habitat classification scheme. Inclusion in the <em>Ambystoma jeffersonianum</em> polyploid complex was based on information from Robertson et al. (2006), Lowcock et al. (1991), and Bogart and Lichts (1986). The presence of the species in a cave environment was based on information from Briggler (2007), Jones and Thompson (1983), Sunny et al. (2014), Gorički et al. (2019), and Ryk (2019). We did not include reports of the species from undercut riverbanks as cave-living, as although semi-enclosed, these represent a microhabitat within a river quite distinct from caves as relevant to our hypothesis. Data on neoteny were collected from amphibiaweb.org and Everson et al. (2021) and coded as a categorical variable with three levels: no neoteny (metamorphosing into terrestrial adults), facultative neoteny, and obligate neoteny. This initial three-state variable is herein referred to as “frequency of neoteny”. For our analyses, we considered three further alternative variables by recoding our initial three-state variable. The recoded variables considered were ‘neoteny’ (pooling facultative or obligate neoteny), ‘facultative neoteny’ (binary variable distinguishing facultative neoteny from both no and obligate neoteny), and obligate neoteny (binary variable distinguishing obligate neoteny from both no and facultative neoteny). We chose to use these alternative variables because it is possible that some of the proposed hypotheses might apply to (e.g.) obligate neoteny only, facultative neoteny, or any degree of neoteny (either as if they were the same thing or in an ordered way with obligate neoteny more extreme than facultative). Hence, using our multiple coding scheme strategy enables a more in-depth evaluation of the hypotheses and under what conditions they might apply.
description: # The neoteny Goldilocks zone: The evolution of neoteny in *Ambystoma*
 [https://doi.org/10.5061/dryad.37pvmcvt0](https://doi.org/10.5061/dryad.37pvmcvt0) This data was used for our study of the same name, to test previously proposed theories of the drivers of neoteny across the genus *Ambystoma*. We also tested the effect of frequency of neoteny on the diversity of habitats a species can occupy, as well as the transition rates from non-neotenic, facultatively neotenic, and obligate neotenic states. Phylogenetic comparative methods used binomial phyloGLMs tested with a tree downloaded from vertlife.org (Jetz and Pyron 2014), to test elevational (stated in meters in the dataset as "MaxElev"), latitudinal distribution (northern and southern distribution limits "NLim" and "SLim", by latitude), cave-associated isolation ("cave", as binomial, with 1 representing species known to occupy caves), and hybridisation-related polyploidy's ("complex", as binomial, with 1 representing species possessing hybridisation related polyploidy) effect on the presence of neoteny ("Neo", as binomial, with 1 representing species that express neoteny), and the presence of facultative neoteny ("NeoFac", as binomial, with 1 representing species that express facultative neoteny). The effect of the number of habitats ("habs", stated by IUCN) was tested against the relative frequency of neoteny ("neoteny", 1- no neoteny, 2-facultative, 3-obligate). Our results suggest that evolutionary transitions between non-neotenic and facultative neoteny states occur at relatively high and approximately equal rates. Moreover, we estimate that obligate neoteny cannot evolve directly from non-neotenic species (and vice versa), such that facultative neoteny acts as an evolutionary ‘stepping stone’ to and from obligate neoteny. However, our transition rate estimates suggest that obligate neoteny is lost &gt;4-times faster than it evolves, partly explaining the rarity of obligate species. These results support the hypothesis that low latitudes favour the evolution of neoteny, presumably linked to more stable (aquatic) environments due to reduced seasonality, but once evolved it may constrain the diversity of habitats.