Testing for shared biogeographic history in the lower Central American freshwater fish assemblage using comparative phylogeography: concerted, independent, or multiple evolutionary responses?

Abstract

A central goal of comparative phylogeography is determining whether codistributed species experienced (1) concerted evolutionary responses to past geological and climatic events, indicated by congruent spatial and temporal patterns (“concerted-response hypothesis”); (2) independent responses, indicated by spatial incongruence (“independent-response hypothesis”); or (3) multiple responses (“multiple-response hypothesis”), indicated by spatial congruence but temporal incongruence (“pseudocongruence”) or spatial and temporal incongruence (“pseudoincongruence”). We tested these competing hypotheses using DNA sequence data from three livebearing fish species codistributed in the Nicaraguan depression of Central America (Alfaro cultratus, Poecilia gillii, and Xenophallus umbratilis) that we predicted might display congruent responses due to co-occurrence in identical freshwater drainages. Spatial analyses recovered different subdivisions of genetic structure for each species, despite shared finer-scale breaks in northwestern Costa Rica (also supported by phylogenetic results). Isolation-with-migration models estimated incongruent timelines of among-region divergences, with A. cultratus and Xenophallus populations diverging over Miocene–mid-Pleistocene while P. gillii populations diverged over mid-late Pleistocene. Approximate Bayesian computation also lent substantial support to multiple discrete divergences over a model of simultaneous divergence across shared spatial breaks (e.g., Bayes factor [B10] = 4.303 for Ψ [no. of divergences] > 1 vs. Ψ = 1). Thus, the data support phylogeographic pseudoincongruence consistent with the multiple-response hypothesis. Model comparisons also indicated incongruence in historical demography, for example, support for intraspecific late Pleistocene population growth was unique to P. gillii, despite evidence for finer-scale population expansions in the other taxa. Empirical tests for phylogeographic congruence indicate that multiple evolutionary responses to historical events have shaped the population structure of freshwater species codistributed within the complex landscapes in/around the Nicaraguan depression. Recent community assembly through different routes (i.e., different past distributions or colonization routes), and intrinsic ecological differences among species, has likely contributed to the unique phylogeographical patterns displayed by these Neotropical fishes.