Phenotypes in Comparative Phylogeography

Earlier this week, The Molecular Ecologist contributor Bryan McLean posted about the current state of comparative phylogeography (Riddle 2016). He listed several exciting directions that comparative phylogeography is heading, including more research that includes trait data.
As a followup to Bryan’s post, I looked into a few ways that recent studies are bringing together phenotype and comparative phylogeography, and what the field might gain from it. 
The problem

For most comparative phylogeographic studies, concordance is the null hypothesis. By including trait data, we can generate more refined phylogeographic hypotheses. Figure from Papadopoulou and Knowles 2016.

Concordance is the null hypothesis in most comparative phylogeographic studies. By including trait data, we can generate more refined phylogeographic hypotheses. Figure from Papadopoulou and Knowles 2016.

The standard approach to comparative phylogeography assumes concordance (i.e., that a biogeographic barrier will cause the same spatial and temporal divergence patterns in multiple species). Discordance is generally regarded as uninteresting or stochastic (Papadoloudou and Knowles 2016).
But disregarding discordance may not always be beneficial or appropriate. A biogeographic barrier may influence multiple species, but to varying degrees depending on phenotype. Phenotypes related to locomotion, physiological tolerance, and body size, for example, can either promote or constrain population divergence (Zamudio et al. 2016).
Instead, it may be valuable to consider discordance, and to ask which traits lead to contrasting responses to biogeographic barriers?
A few recent studies
A study by Papadopoulou and Knowles (2015) was one of the first (that I am aware of) to use trait data to make phylogeographic hypotheses a priori. The authors made trait-based phylogeographic predictions using flightless beetles from a Mediterranean archipelago, then tested the different models using hierarchical approximate Bayesian computation. The 13 co-distributed species they evaluated had different body sizes (which can affect dispersal capacity) and were associated with different soil types (which can affect habitat persistence). The authors found greater support for phylogeographic concordance when body size and soil type were modeled.
Rodríguez et al. (2015) found that forest-dwelling taxa have deeper divergences than species from open habitats.

Rodríguez et al. (2015) found that forest-dwelling taxa have deeper divergences than species from open habitats.

Another case study of tropical anurans (Rodríguez et al. 2015) evaluated phylogeographic structure as it relates to several habitat and natural history traits: body size, macrohabitat type, microhabitat type, reproduction site, climatic heterogeneity, and topographic complexity. The authors found that species inhabiting forests and topographically complex regions (which both likely influence the species’ ability to migrate on the landscape) had deeper phylogeographic structure than species in open habitats.
One other earlier study of three symbiotic fungal species associated with the mountain pine beetle (Roe et al. 2011) identified congruent broad-scale phylogeographic patterns, but fine-scale patterns were incongruent. The authors found that incongruence was linked to specific traits related to transmission mode and environmental tolerance.
Overall, phenotypic traits have been used successfully in many studies to interpret contrasting responses to biogeographic barriers. While trait-based explanations are typically applied ad hoc, I expect that we’ll see more synthetic and rigorous statistical approaches in the near future.
Riddle BR (2016) Comparative phylogeography clarifies the complexity and problems of continental distribution that drove A.R. Wallace to favor islands. PNAS 113(29): 7970-7977. doi: 10.1073/pnas.1601072113
Papadopoulou A and Knowles LL (2016) Toward a paradigm shift in comparative phylogeography driven by trait-based hypotheses. PNAS 113(29): 8018-8024. doi: 10.1073/pnas.1601069113
Zamudio KR, Bell RC, and Mason NA (2016) Phenotypes in phylogeography: Species traits, environmental variation, and vertebrate diversification. PNAS 113(29): 8041-8048. doi: 10.1073/pnas.1602237113
Papadopoulou A and Knowles LL (2015) Species-specific responses to island connectivity cycles: Refined models for testing phylogeographic concordance across a Mediterranean Pleistocene Aggregate Island Complex. Molecular Ecology 24(16):4252-4268. doi: 10.1111/mec.13305
Rodríguez A, et al. (2015) Genetic divergence in tropical anurans: Deeper phylogeographic structure in forest specialists and in topographically complex regions. Evolutionary Ecology 29(5):765-785. doi: 10.1007/s10682-015-9774-7
Roe AD, Rice AV, Coltman DW, Cooke JEK, Sperling FAH (2011) Comparative phylogeography, genetic differentiation and contrasting reproductive modes in three fungal symbionts of a multipartite bark beetle symbiosis. Molecular Ecology 20(3):584-600. doi: 10.1111/j.1365-294X.2010.04953.x

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