Terrestriality constrains salamander limb diversification: Implications for the evolution of pentadactyly

Abstract

Patterns of phenotypic evolution can abruptly shift as species move between adaptive zones. Extant salamanders display three distinct life cycle strategies that range from aquatic to terrestrial (biphasic), to fully aquatic (paedomorphic) and to fully terrestrial (direct development). Life cycle variation is associated with changes in body form such as loss of digits, limb reduction or body elongation. However, the relationships among these traits and life cycle strategy remain unresolved. Here, we use a Bayesian modelling approach to test whether life cycle transitions by salamanders have influenced rates, optima and integration of primary locomotory structures (limbs and trunk). We show that paedomorphic salamanders have elevated rates of limb evolution with optima shifted towards smaller size and fewer digits compared to all other salamanders. Rate of hindlimb digit evolution is shown to decrease in a gradient as life cycles become more terrestrial. Paedomorphs have a higher correlation between hindlimb digit loss and increases in vertebral number, as well as reduced correlations between limb lengths. Our results support the idea that terrestrial plantigrade locomotion constrains limb evolution and, when lifted, leads to higher rates of trait diversification and shifts in optima and integration. The basic tetrapod body form of most salamanders and the independent losses of terrestrial life stages provide an important framework for understanding the evolutionary and developmental mechanisms behind major shifts in ecological zones as seen among early tetrapods during their transition from water to land.

Metamorphosis shapes cranial diversity and rate of evolution in salamanders

“…Changes in developmental strategy are consistently associated with shifts in rate of cranial evolution, with paedomorphic and biphasic species showing faster rates than terrestrial direct-developing species. Furthermore, a reversal from a terrestrial biphasic to an aquatic paedomorphic life cycle is also accompanied by an increase in the rate of cranial evolution, as found in Ledbetter 33 . These results suggest that the rapid morphological evolution in paedomorphic taxa, which tend to live in inhospitable environments with poor access to food resources and mates (such as caves or organic muck habitats) 31,43 , may facilitate the persistence of these species in such challenging conditions 44,45 .…”

“…Changes in developmental strategy have impacted the dynamics of body form and limb evolution in salamanders over the last ~160My 25,33 . As shown in previous studies, a biphasic life cycle was recovered as the ancestral condition for Caudata 41,42 , with direct-development evolving once, paedomorphy evolving several times independently 25,29,31 , and biphasic (and sometimes then paedomorphic) strategies evolving and re-evolving multiple times among direct-developing plethodontids.…”

“…Among the organisms experiencing metamorphosis, salamanders (Amphibia: Caudata, ~ 700 species 27,28 ) display a tremendous diversity of species, ecologies and life cycles with multiple independent evolutions thereof 25,[29][30][31][32][33] . Thus, salamanders provide an excellent framework to study how developmental processes can produce morphological diversity.…”

“…They also found that constraints on body form evolution are stage-specific and that shifts in life cycle complexity can alter the dynamics of morphological evolution in salamanders. Ledbetter and Bonett 33 showed that limbs evolve faster and are less constrained for aquatic species (mostly paedomorphic) than terrestrial species (mostly direct-developing). Vučić, et al 26 demonstrated that metamorphosis cannot be regarded as a developmental constraint on the overall external head in a newt.…”

Cranial integration in the fire salamander, Salamandra salamandra (Caudata: Salamandridae)

“…Thus investigation into finer-scale patterns of static and evolutionary integration for additional lissamphibian groups may reveal whether this pattern is conserved across Lissamphibia. Caudata (salamanders) comprises 10 ecologically and morphologically diverse families and displays a tremendous range of life cycle strategies (e.g., Bonett, 2018;Bonett & Blair, 2017;Bonett et al, 2013;Ledbetter & Bonett, 2019). Extensive phenotypic variation can also extend intraspecifically in salamanders, as in the fire salamander Salamandra salamandra (Linnaeus, 1758) which exhibits a range of morphologies, colour patterns and reproductive strategies depending on the subspecies (Sparreboom, 2014;Beukema et al, 2016).…”