Evolutionary diversification of cryophilic Grylloblatta species (Grylloblattodea: Grylloblattidae) in alpine habitats of California

Abstract

Background: Climate in alpine habitats has undergone extreme variation during Pliocene and Pleistocene epochs, resulting in repeated expansion and contraction of alpine glaciers. Many cold-adapted alpine species have responded to these climatic changes with long-distance range shifts. These species typically exhibit shallow genetic differentiation over a large geographical area. In contrast, poorly dispersing organisms often form species complexes within mountain ranges, such as the California endemic ice-crawlers (Grylloblattodea: Grylloblattidae: Grylloblatta). The diversification pattern of poorly dispersing species might provide more information on the localized effects of historical climate change, the importance of particular climatic events, as well as the history of dispersal. Here we use multi-locus genetic data to examine the phylogenetic relationships and geographic pattern of diversification in California Grylloblatta.

Results: Our analysis reveals a pattern of deep genetic subdivision among geographically isolated populations of Grylloblatta in California. Alpine populations diverged from low elevation populations and subsequently diversified. Using a Bayesian relaxed clock model and both uncalibrated and calibrated measurements of time to most recent common ancestor, we reconstruct the temporal diversification of alpine Grylloblatta populations. Based on calibrated relaxed clock estimates, evolutionary diversification of Grylloblatta occurred during the Pliocene-Pleistocene epochs, with an initial dispersal into California during the Pliocene and species diversification in alpine clades during the middle Pleistocene epoch.

Conclusions: Grylloblatta species exhibit a high degree of genetic subdivision in California with well defined geographic structure. Distinct glacial refugia can be inferred within the Sierra Nevada, corresponding to major, glaciated drainage basins. Low elevation populations are sister to alpine populations, suggesting alpine populations may track expanding glacial ice sheets and diversify as a result of multiple glacial advances. Based on relaxed-clock molecular dating, the temporal diversification of Grylloblatta provides evidence for the role of a climate-driven species pump in alpine species during the Pleistocene epoch.

Figure 1

Sampling locations of Grylloblatta. Location of sampled Grylloblatta populations in California and Oregon, overlaid on an mean minimum annual temperature surface for 1971-2000 [81] and an outline of glacial ice extent during the last glacial maximum [82]. Type localities of species indicated with an asterisk.

Figure 2

Bayesian phylogeny of California Grylloblatta. Concatenated phylogeny with Bayesian posterior probability support values shown at the nodes. Nodes conflicting with the maximum likelihood topology indicated by asterisks and low elevation populations indicated by shading in gray. Sample site numbers follow names at tips.

Figure 3

Maximum likelihood phylogeny of California Grylloblatta. Maximum likelihood topology based on 1000 bootstrap replicates. Nodes conflicting with the Bayesian topology indicated by asterisks and low elevation populations indicated by shading in gray. Sample site numbers follow names at tips.

Figure 4

Geographic distribution of alpine Grylloblatta lineages. A) Geographic distribution of genetically distinct alpine lineages in the Sierra Nevada overlaid on a topographic base map of California [82]. B) Adult female Grylloblatta sp. from the White Mountains.