Similar but different: Revealing the relative roles of species‐traits versus biome properties structuring genetic variation in South American marsh rats

Abstract

Aim Wetland habitats, and the ecological restrictions imposed by them, structure patterns of genetic variation in constituent taxa. As such, genetic variation may reflect properties of the specific biomes species inhabit, or shared life history traits among species may result in similar genetic structure. We evaluated these hypotheses jointly by quantifying the similarity of genetic structure in three South American marsh rat species (Holochilus), and test how genetic variation in each species relates to biome‐specific environmental space and historical stability. Location South America. Taxon Rodentia. Methods Using complementary analyses (Mantel tests, dbRDA, Procrustes, covariance structure of allele frequencies and environmental niche models [ENMs]) with 8,000–32,000 SNPs per species, we quantified the association between genomic variation and geographic and/or environmental differences. Results Significant association between genetic variation and geography was identified for all species. Similarity in the strength of the association suggests connectivity patterns dictated by shared species‐traits predominate at the biome scale. However, substantial amounts of genetic variation are not explained by geography. Focusing on this portion of the variance, we demonstrate a significant quantitative association between genetic variation and the environmental space of a biome, and a qualitative association with varying regional stability. Specifically, historically stable areas estimated from ecological niche models are correlated with local levels of geographic structuring, suggesting that local biome‐specific histories affect population isolation/connectivity. Main conclusions These tests show that although species exhibit similar patterns of genetic variation that are consistent with shared natural histories, irrespective of inhabiting different wetland biomes, local biome‐specific properties (i.e. varying environmental conditions and historical stability) contribute to departures from equilibrium patterns of genetic variation expected by isolation by geographic distance. The reflection of these biome‐specific properties in the genetic structure of the marsh rats provides a window into the differences among South American wetlands with evolutionary consequences for their respective constituent assemblages.

Genetic variation of the Chilean endemic long-haired mouseAbrothrix longipilis(Rodentia, Supramyomorpha, Cricetidae) in a geographical and environmental context

“…In this study, we assessed the genetic variation of Abrothrix longipilis using information contained in sequences of the mitochondrial gene Cytb and a wide panel of SNPs. RNA-seq remains as a underutilized approach to acquire larger amounts of nuclear sequence data in sigmodontine studies (see Giorello et al, 2018 ; Prado et al, 2019 for the two so far available studies). In this sense, we are paving the way for the much needed transition to the genomic era of the study of South American rodents (see also Valdez et al, 2015 ; Giorello et al, 2018 ), as a way to deepen the understanding of the patterns and processes that underlie rodent diversity (see claims in this line in Lessa et al (2014) and D’Elía, Fabre & Lessa (2019) ).…”

Functional connectivity in sympatric spiny rats reflects different dimensions of Amazonian forest‐association

“…This indicates that there are factors that were not explicitly tested in our study. It is possible that the association between gene and geography on a regional scale relates to variation in the historical stability of the South American wetlands (Prado et al, 2019). However, studies have shown little variation in precipitation (Cheng et al, 2013), temperature (Colinvaux et al, 1996) and vegetation (Häggi et al, 2017) since the last glacial maximum (Pleistocene) in the Western Amazon.…”

“…The following genetic diversity metrics were calculated for each GC identified in each species: expected heterozygosity (HE EXP ), nucleotide diversity ( π ), and inbreeding coefficient ( F IS ), using the Query function available in “r2vcftools” 0.0.0.9 (Pope, 2020). Tests of significant differences in diversity values (among species and among GCs) were assessed with Tukey's test using Query function as well (see Prado et al, 2019). In addition, F ST (SNP‐based F ‐statistics) was used to measure genetic differentiation between GCs using the gl.fst.pop function in “dartR” 1.9.9.1 (Gruber & Georges, 2019) with 100 bootstraps.…”

“…South American wetlands (Prado et al, 2019). However, studies have shown little variation in precipitation (Cheng et al, 2013), temperature (Colinvaux et al, 1996) and vegetation (Häggi et al, 2017) since the last glacial maximum (Pleistocene) in the Western Amazon.…”

“…The effects of the landscape on the dispersal of organisms are understood as functional connectivity, given that it's not geographical distance alone that determines gene flow, but also how organisms perceive and respond to landscape structure (Manel & Holderegger, 2013). As such, the divergence process may differ among sympatric taxa when the species’ ecologies affect connectivity among populations because of differences in how they perceive and respond to the landscape (Pirani et al, 2019), in addition to differences in the landscape structure of different habitat types (Massatti & Knowles, 2016; Prado et al, 2019).…”