Divergent selection along elevational gradients promotes genetic and phenotypic disparities among small mammal populations

Abstract

Species distributed along mountain slopes, facing contrasting habitats in short geographic scale, are of particular interest to test how ecologically based divergent selection promotes phenotypic and genetic disparities as well as to assess isolation‐by‐environment mechanisms. Here, we conduct the first broad comparative study of phenotypic variation along elevational gradients, integrating a large array of ecological predictors and disentangling population genetic driver processes. The skull form of nine ecologically distinct species distributed over a large altitudinal range (100–4200 m) was compared to assess whether phenotypic divergence is a common phenomenon in small mammals and whether it shows parallel patterns. We also investigated the relative contribution of biotic (competition and predation) and abiotic parameters on phenotypic divergence via mixed models. Finally, we assessed the population genetic structure of a rodent species (Niviventer confucianus) via analysis of molecular variance and FST along three mountain slopes and tested the isolation‐by‐environment hypothesis using Mantel test and redundancy analysis. We found a consistent phenotypic divergence and marked genetic structure along elevational gradients; however, the species showed mixed patterns of size and skull shape trends across mountain zones. Individuals living at lower altitudes differed greatly in both phenotype and genotype from those living at high elevations, while middle‐elevation individuals showed more intermediate forms. The ecological parameters associated with phenotypic divergence along elevation gradients are partly related to species' ecological and evolutionary constraints. Fossorial and solitary animals are mainly affected by climatic factors, while terrestrial and more gregarious species are influenced by biotic and abiotic parameters. A novel finding of our study is that predator richness emerged as an important factor associated with the intraspecific diversification of the mammalian skull along elevational gradients, a previously overlooked parameter. Population genetic structure was mainly driven by environmental heterogeneity along mountain slopes, with no or a week spatial effect, fitting the isolation‐by‐environment scenario. Our study highlights the strong and multifaceted effects of heterogeneous steep habitats and ecologically based divergent selective forces in small mammal populations.

Ecological Factors Generally Not Altitude Related Played Main Roles in Driving Potential Adaptive Evolution at Elevational Range Margin Populations of Taiwan Incense Cedar (Calocedrus formosana)

“…Geography and environment can both be effective barriers to gene flow between populations ( Hahn et al, 2012 ; Wang et al, 2013 ; Sexton et al, 2014 ; Reis et al, 2015 ; Antonelli, 2017 ; Feijó et al, 2019 ). These factors are not mutually exclusive and they are closely related directly or indirectly influencing the process of dispersal ( Wang et al, 2013 ; Huang et al, 2016 ), and we are expecting to find both geography and environment explaining the outlier genetic variation to a certain degree.…”

Drivers of population divergence and species differentiation in a recent group of indigenous orchids (Vanilla spp.) in Madagascar

“…However, they can also be an important force driving genetic differentiation and speciation (Hewitt, 1996; Vences et al., 2009). For example, climatic variations along latitudinal gradients may affect organism functional traits such as phenology (Olsson & Ågren, 2002), physiology (Bognounou et al., 2010; De Frenne et al., 2012), and morphology (Feijó et al., 2019; Olsson & Ågren, 2002; Winn & Gross, 1993) and lead to plastic or genotypic shifts (Byars et al., 2007). Correlation analysis of neutral genetic variations versus geographic distances allows testing for IBD.…”

Divergent adaptations in resource‐use traits explain how pikas thrive on the roof of the world

“…Specifically, we assess cranial evolution of Ochotona using geometric morphometric and phylogenetic comparative techniques to ask whether adaptations among high-elevation biota shown at the molecular and physiological levels also occur in resource-use phenotypic traits. We expect that species living at distinct altitudinal levels will show dissimilar morphological strategies to cope with distinct selection pressures, as recently shown at the population level for small mammals (Feijó et al, 2019).…”

“…Resourceuse phenotypic adaptations associated with restrictive habitats are well documented in subterranean (Da Silva et al, 2018;Marcy, Hadly, Sherratt, Garland, & Weisbecker, 2016;Sherratt, Gower, Klingenberg, & Wilkinson, 2014), rock-dwelling (Collar, Schulte, O'Meara, & Losos, 2010;Goodman, Miles, & Schwarzkopf, 2008;Revell, Johnson, Schulte, Kolbe, & Losos, 2007) and desert (Alhajeri & Steppan, 2018) animals. However, the few existing empirical studies on high-elevation morphological adaptations are mostly limited to intraspecific variation along mountain slopes, focusing on cold and desiccation tolerance (reviewed by Keller, Alexander, Holderegger, & Edwards, 2013; but see Feijó et al, 2019), lacking a macroevolutionary perspective. By focusing on only one level of adaptation (cellular), we are likely to overlook key evolutionary and ecological responses that allow animals to cope with multiple stresses in extreme-elevation environments.…”