Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses

Abstract

For three decades, comparative phylogeography has conceptually and methodologically relied on the concordance criterion for providing insights into the historical/biogeographic processes driving population genetic structure and divergence. Here we discuss how this emphasis, and the corresponding lack of methods for extracting information about biotic/intrinsic contributions to patterns of genetic variation, may bias our general understanding of the factors driving genetic structure. Specifically, this emphasis has promoted a tendency to attribute discordant phylogeographic patterns to the idiosyncracies of history, as well as an adherence to generic null expectations of concordance with reduced predictive power. We advocate that it is time for a paradigm shift in comparative phylogeography, especially given the limited utility of the concordance criterion as genomic data provide ever-increasing levels of resolution. Instead of adhering to the concordance-discordance dichotomy, comparative phylogeography needs to emphasize the contribution of taxon-specific traits that will determine whether concordance is a meaningful criterion for evaluating hypotheses or may predict discordant phylogeographic structure. Through reference to some case studies we illustrate how refined hypotheses based on taxon-specific traits can provide improved predictive frameworks to forecast species responses to climatic change or biogeographic barriers while gaining unique insights about the taxa themselves and their interactions with their environment. We outline a potential avenue toward a synthetic comparative phylogeographic paradigm that includes addressing some important conceptual and methodological challenges related to study design and application of model-based approaches for evaluating support of trait-based hypotheses under the proposed paradigm.biogeography | ecological traits | coalescent modeling | Pleistocene | statistical phylogeography P aralleling its critical role in identifying biogeographic phenomena by common structuring of genetic variation across taxa, comparative phylogeography has the potential to offer unprecedented insights about the taxa themselves. We here make an argument that such a paradigm shift, in which the contribution of biotic attributes are a focal point, as opposed to an emphasis on abiotic factors, is not only a valuable endeavor in itself, but it is also critical to (i) understanding the relative contributions of abiotic/extrinsic (e.g., geography, geological, or climatic history) vs. biotic/intrinsic (e.g., ecological or life history traits; hereafter referred to as biotic) factors in structuring genetic variation and divergence across taxa, as well as (ii) determining the relative prevalence of deterministic processes versus stochasticity in the evolutionary history of taxa, and we argue that (iii) the key to meaningful insights is not just a function of the statistical support we might have for a model, but it also depends on the creativity of biologists to identify hypotheses that are releva...

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

“…An important advance in this direction is the development of model-based phylogeographic methods that incorporate phenotypic variation. These efforts stem from the realization that lack of concordance in temporal and spatial clustering in codistributed taxa may not mean that taxa are not responding to a common landscape or climatic barrier (32); rather, discrepancies may reflect variation in ecological traits and dispersal capabilities of taxa sampled across the presumed barrier (33). These efforts refine expectations for spatial concordance and temporally clustered divergences by explicitly including geography and trait-based responses for each species (27).…”

“…This exciting prospect will greatly increase the impact of phylogeography in biodiversity science, and future studies need to consider explicitly how phenotypes can be incorporated into their predictive frameworks. Just as common responses to phylogeographic barriers became a null hypothesis early in the history of the field (33), an understanding of how organismal traits mediate responses to variable environments and demography will be necessary for a complete picture of the expected mode and rate of phylogeographic diversification (22). Achieving this understanding will require the development of metrics for quantifying phenotypic divergence and methods that explicitly incorporate those data in phylogeographic predictions and analyses (34).…”

“…One prominent goal of phylogeography is to infer the biological mechanisms that partition genetic and phenotypic variation among populations. Recent advances in modeling (37), predictive frameworks for incorporating phenotypes into phylogeography (33), and DNA sequencing technologies (7) have bolstered our ability to identify and quantify the mechanisms that generate this diversity. Here, we illustrate those biological mechanisms that favor spatial concordance (or discordance) of genetic and phenotypic variation within a phylogeographic framework.…”

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

“…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.…”

In the light of evolution X: Comparative phylogeography

“…Rissler concludes by advocating a union of comparative phylogeography and landscape genetics under the broader umbrella of biogeography, which has always sought to connect ecology and evolutionary biology. The union of comparative phylogeography and biogeography is a theme that emerged in the first contribution (19), was elaborated throughout this colloquium (26,29, and elsewhere), and is eloquently summarized in this final contribution (34).…”