Contrasting support for alternative models of genomic variation based on microhabitat preference: species‐specific effects of climate change in alpine sedges

Abstract

Deterministic processes may uniquely affect codistributed species' phylogeographic patterns such that discordant genetic variation among taxa is predicted. Yet, explicitly testing expectations of genomic discordance in a statistical framework remains challenging. Here, we construct spatially and temporally dynamic models to investigate the hypothesized effect of microhabitat preferences on the permeability of glaciated regions to gene flow in two closely related montane species. Utilizing environmental niche models from the Last Glacial Maximum and the present to inform demographic models of changes in habitat suitability over time, we evaluate the relative probabilities of two alternative models using approximate Bayesian computation (ABC) in which glaciated regions are either (i) permeable or (ii) a barrier to gene flow. Results based on the fit of the empirical data to data sets simulated using a spatially explicit coalescent under alternative models indicate that genomic data are consistent with predictions about the hypothesized role of microhabitat in generating discordant patterns of genetic variation among the taxa. Specifically, a model in which glaciated areas acted as a barrier was much more probable based on patterns of genomic variation in Carex nova, a wet-adapted species. However, in the dry-adapted Carex chalciolepis, the permeable model was more probable, although the difference in the support of the models was small. This work highlights how statistical inferences can be used to distinguish deterministic processes that are expected to result in discordant genomic patterns among species, including species-specific responses to climate change.

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

“…Of course when designing a study, especially for model-based tests (16), it is imperative that the biological processes of interest are represented by the suite of hypotheses tested, as there is no way to rule out additional hypotheses that have not been evaluated. Phylogeographic analyses do not identify "the evolutionary history" of taxa per se (56), instead the insights of model-based approaches rest with demonstrating the relative support of one hypothesis relative to others where each of the different hypotheses relevant to evaluating a question are represented in the study (24). The proposed paradigm shift in comparative phylogeography will require an appropriate statistical framework to accommodate and interpret phylogeographic discordance.…”

“…Likewise, potential problems might be introduced when translating biological hypotheses into models for statistical tests. Specifically, the support (or lack thereof) for alternative hypotheses might reflect differences in the extent to which taxa conform to assumptions used to generate species-specific predictions, rather than key differences in the models themselves (24).…”

“…Even though it might be possible to compare large sets of hypotheses without using any a priori biological knowledge of the study system (60,61), that might not be particularly meaningful. The insights provided by selecting one model over another will be limited if the models only vary in nonkey parameters that do not make any important difference for their biological interpretation (24). In other words, without knowing Box 1: Refined vs. Generic Hypotheses in hABC to Evaluate Climate-Driven Diversification hABC analyses are widely used in comparative phylogeography to evaluate scenarios of climate-driven diversification by testing for simultaneous divergence among population pairs of codistributed taxa (12,66,67).…”

“…Different approaches might be used to design comparative phylogeographic studies for testing biologically informed hypotheses. If the goal is to address questions about the possible role of a specific ecological trait in structuring genetic variation, it might be useful to focus on taxa that differ only in the targeted ecological trait (23,24). With such a study design, refined hypotheses of concordance based on taxon-specific traits can be used, thereby providing a better predictive framework for comparative phylogeographic tests (Box 1).…”

“…Moreover, the adherence to the concordance criterion results in tests that are often too generic and thus have reduced predictive power (23), where the rejection of concordance is often met with ad hoc explanations for the observed discordance. Last, without a correspondingly well-developed statistical framework for making predictions about discordance (24), extracting information about biotic contributions to patterns of genetic variation among codistributed species also becomes challenging. This limitation is especially critical given that if species-specific traits actually have a significant impact, then by definition, discordance will characterize genetic variation among codistributed species.…”