Convergent evolution of olfactory and thermoregulatory capacities in small amphibious mammals

Abstract

Olfaction and thermoregulation are key functions for mammals. The former is critical to feeding, mating, and predator avoidance behaviors, while the latter is essential for homeothermy. Aquatic and amphibious mammals face olfactory and thermoregulatory challenges not generally encountered by terrestrial species. In mammals, the nasal cavity houses a bony system supporting soft tissues and sensory organs implicated in either olfactory or thermoregulatory functions. It is hypothesized that to cope with aquatic environments, amphibious mammals have expanded their thermoregulatory capacity at the expense of their olfactory system. We investigated the evolutionary history of this potential trade-off using a comparative dataset of three-dimensional (3D) CT scans of 189 skulls, capturing 17 independent transitions from a strictly terrestrial to an amphibious lifestyle across small mammals (Afrosoricida, Eulipotyphla, and Rodentia). We identified rapid and repeated loss of olfactory capacities synchronously associated with gains in thermoregulatory capacity in amphibious taxa sampled from across mammalian phylogenetic diversity. Evolutionary models further reveal that these convergences result from faster rates of turbinal bone evolution and release of selective constraints on the thermoregulatory-olfaction trade-off in amphibious species. Lastly, we demonstrated that traits related to vital functions evolved faster to the optimum compared to traits that are not related to vital functions.

Locomotory mode transitions alter phenotypic evolution and lineage diversification in an ecologically rich clade of mammals

“…Most amphibious mammals, and amphibious vertebrates in general, swim using hind-foot and tail propulsion (Hickman 1979;Samuels and van Valkenburgh 2008), which is thought to select for elongate hind feet and powerful, long tails that are often laterally compressed or augmented with stiff vertically oriented hairs (Voss 1988;Rowe et al 2014). Our observations of increased HBL, mass, RHF, and RTL support these existing hypotheses of convergent evolution in Amphibious species (Kerbis Peterhans and Patterson 1995;Meiri 2008;Rowe et al 2014;Martinez et al 2020).…”

Incomplete convergence of gliding mammal skeletons*

“…2016; Grossnickle 2020, Martinez et al. 2020). Nonetheless, a more nuanced consideration of our results reveals a lack of evidence for complete convergence, as demonstrated by the phylomorphospace trajectories, divergence among marsupials, model‐fitting results, and elevated morphological disparity of gliders.…”

“…We follow Martinez et al. (2020) in referring to these as “BM1m” models. Although rates are constant across regimes, they are allowed to vary among traits (i.e., the five PCs), which is a default mvMORPH setting.…”

“…2017; Martinez et al. 2020). Although evidence of morphological convergence is often qualitative, recently developed methods provide novel tools for identifying and quantifying convergence (Ingram and Mahler 2013; Arbuckle et al.…”

“…The repeated, convergent evolution of a similar form is commonplace, and it is often used as an indicator of adaptive evolution (Wright 1932;Simpson 1944;Schluter 2000;Losos 2011;Friedman et al 2016;Zelditch et al 2017;Martinez et al 2020). Although evidence of morphological convergence is often qualitative, recently developed methods provide novel tools for identifying and quantifying convergence (Ingram and Mahler 2013;Arbuckle et al 2014;Stayton 2015a;Castiglione et al 2019).…”