Phenotypes in phylogeography: Species’ traits, environmental variation, and vertebrate diversification

Abstract

Almost 30 y ago, the field of intraspecific phylogeography laid the foundation for spatially explicit and genealogically informed studies of population divergence. With new methods and markers, the focus in phylogeography shifted to previously unrecognized geographic genetic variation, thus reducing the attention paid to phenotypic variation in those same diverging lineages. Although phenotypic differences among lineages once provided the main data for studies of evolutionary change, the mechanisms shaping phenotypic differentiation and their integration with intraspecific genetic structure have been underexplored in phylogeographic studies. However, phenotypes are targets of selection and play important roles in species performance, recognition, and diversification. Here, we focus on three questions. First, how can phenotypes elucidate mechanisms underlying concordant or idiosyncratic responses of vertebrate species evolving in shared landscapes? Second, what mechanisms underlie the concordance or discordance of phenotypic and phylogeographic differentiation? Third, how can phylogeography contribute to our understanding of functional phenotypic evolution? We demonstrate that the integration of phenotypic data extends the reach of phylogeography to explain the origin and maintenance of biodiversity. Finally, we stress the importance of natural history collections as sources of high-quality phenotypic data that span temporal and spatial axes.phylogeography | phenotype | function | trait | concordance P hylogeography, as originally defined, focused on processes governing the spatial distribution of genealogical lineages within species (1). One of the strengths of the field at its inception was formalizing conceptual links among heredity (processes at the level of individual pedigrees), divergence at the population level, and phylogenetic relationships among species (1). This analytical framework bridged microevolutionary processes acting within populations and macroevolutionary patterns at larger spatial and temporal scales. From the earliest applications, empirical phylogeographic studies described spatial patterns of genetic diversity and inferred underlying mechanisms, thus contributing to the explanatory and predictive power of the field (2). If most species show phylogeographic structure caused by landscape features that impede gene flow, then the geographic distribution of divergent lineages should coincide among species that coinhabit those landscapes. Further, phylogeographic breaks or contact zones should arise as lineages diverge allopatrically or come into secondary contact after divergence, respectively. This explicit prediction (1) resulted in a search for shared geographic patterns in genetic structure among species and the birth of comparative phylogeography (3, 4). Now, with thousands of taxon-specific phylogeographic studies published and synthesized in comparative studies (5, 6), we have learned a tremendous amount about the geography of genetic structure both within and among species.Phylogeogra...

Inferring responses to climate dynamics from historical demography in neotropical forest lizards

“…This view is supported by tests of synchronous population size shifts that allow for species-specific parameters as well as by plausible models of the distribution of genetic diversity under future carbon emissions. Taxa associated with broadly similar climatic conditions exhibit contrasting responses to common environmental changes, a scenario also supported by simulationbased macroecological studies (20).…”

“…If idiosyncratic responses to common landscape changes characterize ecological communities in the tropics (17,18) and beyond (19,20), their incorporation in phylogeographic methods can significantly improve our understanding of the impacts of former environmental shifts on regional species pools. Methods that build upon coalescent theory to account for historical heterogeneity across taxa under a single statistical framework (21,22) provide increased power to test concerted demographic responses at the level of ecological assemblages.…”

Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

“…(2006) coined the term “phenogeography” to study the distribution and the genetic basis of phenotypic variation in nature as opposed to phylogeography (i.e., the geography of phenotypic variation vs the geography of lineages). The integration of phenogeography and phylogeography should contribute to better understanding of functional phenotypic evolution, and then fitness performance within and among lineages (Zamudio, Bell, & Mason, 2016). However, phenogeography—with the noticeable exception of counter‐ and cogradient variation studies (Conover, Duffy, & Hice, 2009; Hice, Duffy, Munch, & Conover, 2012) and few Q ST ‐F ST studies (DeFaveri & Merilä, 2013)—remains largely neglected in marine species.…”

Neutral and functionally important genes shed light on phylogeography and the history of high‐altitude colonization in a widespread New World duck

“…Specifically, relative to previous analysis, our addition of samples from the Colombian Andes to phylogeographic analyses revealed (1) that the direction of colonization of Ruddy Ducks appears more difficult to determine—and may even be opposite—than that which was previously inferred, and (2) that if adjustment to high‐elevation conditions played an important role in colonization of new areas by Ruddy Ducks, it likely occurred through different adaptive mechanisms than those previously considered or via phenotypic plasticity in physiological parameters that remain to be studied. In any event, our study also exemplifies the breadth of inferences about species history one can potentially make by combining data from nuclear and functionally important loci in phylogeography (Zamudio et al., 2016). …”

“…However, genes of functional importance can also be employed to investigate the history of species, particularly when populations are exposed to distinct environments with contrasting selective pressures (Deagle, Jones, Absher, Kingsley, & Reimchen, 2013; Feldman, Brodie, & Pfrender, 2009; Hoekstra, Drumm, & Nachman, 2004; Savage & Zamudio, 2016; Sork et al., 2016). Analyses of functionally important genes allow one to address questions about evolutionary processes such as adaptation and natural selection, complementing inferences of demographic processes based on patterns of geographic variation in neutral genes (Zamudio, Bell, & Mason, 2016). Here, we integrate analyses of neutral markers and protein‐coding genes potentially under selection to test hypotheses about the biogeographic and evolutionary history of a widespread species of duck with a broad latitudinal and elevational distribution in the New World.…”