Macroevolution of desiccation‐related morphology in plethodontid salamanders as inferred from a novel surface area to volume ratio estimation approach

Abstract

Evolutionary biologists have long been interested in the macroevolutionary consequences of various selection pressures, yet physiological responses to selection across deep time are not well understood. In this paper, we investigate how a physiologically relevant morphological trait, surface area to volume ratio (SA:V) of lungless salamanders, has evolved across broad regional and climatic variation. SA:V directly impacts an organisms’ ability to retain water, leading to the expectation that smaller SA:Vs would be advantageous in arid, water‐limited environments. To explore the macroevolutionary patterns of SA:V, we first develop an accurate method for estimating SA:V from linear measurements. Next, we investigate the macroevolutionary patterns of SA:V across 257 salamander species, revealing that higher SA:Vs phylogenetically correlate with warmer, wetter climates. We also observe higher SA:V disparity and rate of evolution in tropical species, mirrored by higher climatic disparity in available and occupied tropical habitats. Taken together, these results suggest that the tropics have provided a wider range of warmer, wetter climates for salamanders to exploit, thereby relaxing desiccation pressures on SA:V. Overall, this paper provides an accurate, efficient method for quantifying salamander SA:V, allowing us to demonstrate the power of physiological selection pressures in influencing the macroevolution of morphology.

Rapid phenotypic change in a polymorphic salamander over 43 years

“…However, the environmental conditions that lure the larger unstriped morphs to the surface remain unclear. Further work examining body size variation between color morphs would benefit from evaluation of surface area to volume ratios of morphs 83 , in addition to trunk vertebrae counts, which is the known mechanism of elongation in Plethodon 84 . We collected digital x-rays for a small subset of salamanders included in our study, and these data indicate that counting vertebrae is a feasible next step for further exploring the divergence in body size between the morphs.…”

Is salamander arboreality limited by broad-scale climatic conditions?

“…First, it is well-established that local environmental conditions influence plethodontid landscape movement and short-term microhabitat selection [7][8][9][10][11][12]. Second, Baken and colleagues [13] revealed a strong correlation between broad climatic patterns and plethodontid surface area to volume ratio (SA:V) evolution, demonstrating the power of climate to influence macroevolutionary patterns within this family. Finally, SA:V, the trait shown to be tied to climatic variation, is directly related to two physiological demands that are amplified by arboreal life: moisture conservation and oxygen acquisition.…”

Genome size influences adaptive plasticity of water loss, but not metabolic rates, in lungless salamanders

“…4A), coincident with decreases in all our water loss responses, a pattern indicative of plasticity in r across temperatures. Given the selective strength of desiccation risk in plethodontids (Baken et al, 2020;Feder, 1983) and the ecological importance of minimizing water loss (Feder, 1983;Riddell et al, 2018), this result suggests that plasticity in r is adaptive at higher temperatures (Ghalambor et al, 2007). The significant mediation of C-value in our path models at 15°C thus implies that genome size mechanistically influences increased resistance to water loss under warmer conditions.…”

“…In terrestrial taxa, selection for this plasticity should be strongest where desiccation risk is greatest, placing tighter constraints on C-value evolution in drier climates. Intriguingly, the contribution of random drift to variation in plethodontid genome size is most evident in the Neotropics (Itgen et al, 2019), an environment defined by selective release from desiccation risk (Baken et al, 2020). Thus, selection on genome size is probably stronger in temperate species more prone to evaporative water loss.…”