The neoteny Goldilocks zone: The evolution of neoteny in Ambystoma

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 > 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.