Comparative Phylogeography of a Coevolved Community: Concerted Population Expansions in Joshua Trees and Four Yucca Moths

Abstract

Comparative phylogeographic studies have had mixed success in identifying common phylogeographic patterns among co-distributed organisms. Whereas some have found broadly similar patterns across a diverse array of taxa, others have found that the histories of different species are more idiosyncratic than congruent. The variation in the results of comparative phylogeographic studies could indicate that the extent to which sympatrically-distributed organisms share common biogeographic histories varies depending on the strength and specificity of ecological interactions between them. To test this hypothesis, we examined demographic and phylogeographic patterns in a highly specialized, coevolved community – Joshua trees (Yucca brevifolia) and their associated yucca moths. This tightly-integrated, mutually interdependent community is known to have experienced significant range changes at the end of the last glacial period, so there is a strong a priori expectation that these organisms will show common signatures of demographic and distributional changes over time. Using a database of >5000 GPS records for Joshua trees, and multi-locus DNA sequence data from the Joshua tree and four species of yucca moth, we combined paleaodistribution modeling with coalescent-based analyses of demographic and phylgeographic history. We extensively evaluated the power of our methods to infer past population size and distributional changes by evaluating the effect of different inference procedures on our results, comparing our palaeodistribution models to Pleistocene-aged packrat midden records, and simulating DNA sequence data under a variety of alternative demographic histories. Together the results indicate that these organisms have shared a common history of population expansion, and that these expansions were broadly coincident in time. However, contrary to our expectations, none of our analyses indicated significant range or population size reductions at the end of the last glacial period, and the inferred demographic changes substantially predate Holocene climate changes.

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

“…Commonly applied tests include the evaluation of spatially concordant phylogeographic breaks (10,11), temporally synchronous population divergence (12,13), or concerted demographic expansion/contraction (14,15) among members of an ecological community. Methodological advances of the last decade, especially coalescent-based tools for hypothesis testing and parameter estimation (16,17) that include statistical assessment of concordance across taxa, such as the widely used hierarchical approximate Bayesian computation (hABC) This article is a PNAS Direct Submission.…”

Population-level genetic variation and climate change in a biodiversity hotspot

“…Comparative phylogeographic studies among Yucca brevifolia, two obligate pollinators (Tegeticula antithetica and Tegeticula synthetica) and two species of parasitizing yucca moths (Prodoxus weethumpi and Prodoxus sordidus) provides evidence for the effects of climate change on species distributions and genetic structure (Smith et al, 2011). Coalescentbased DNA sequence analyses and distribution modelling of Y. brevifolia trees since the Last Glacial Maximum (LGM) indicate that demographic changes in all species were present prior to climatic change during the Holocene (Smith et al, 2011).…”

“…Coalescentbased DNA sequence analyses and distribution modelling of Y. brevifolia trees since the Last Glacial Maximum (LGM) indicate that demographic changes in all species were present prior to climatic change during the Holocene (Smith et al, 2011). For the insect species some divergence is apparent, with average F ST values of 0Á12; however, Y. brevifolia variation is quite different, with high global F ST values of 0Á87, which strongly correlate with geographic distance, which is structured by pollinator association.…”

“…Pleistocene glaciations throughout California were significant forces affecting intraspecific, interspecific and intergeneric evolutionary patterns in plants and animals, particularly those with low dispersal ability. In contrast, the Klamath-Siskiyou region experienced minimal glaciation and served as a refugium for many plant taxa (Smith and Sawyer, 1988;Soltis et al, 1997;Sawyer, 2006).…”

Phylogeographic model selection leads to insight into the evolutionary history of four-eyed frogs

“…[12][13][14] or to test phylogeographic hypotheses against a null model (e.g., refs. [15][16][17]. Such methods have been widely adopted by the phylogeographic community because model-based methods offer a path toward estimating putatively relevant parameters, and because the models themselves can be tailored to the particulars of a given system (e.g., refs.…”