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Species Divergence During Rapid Climate Change

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Species Divergence During Rapid Climate Change Molecular Ecology (2007) 16, 619–627 doi: 10.1111/j.1365-294X.2006.03167.x ShiftingBlackwell Publishing Ltd distributions and speciation: species divergence during rapid climate change BRYAN C. CARSTENS and L. LACEY KNOWLES Department of Ecology & Evolutionary Biology, 1109 Geddes Ave., Museum of Zoology, Room 1089, University of Michigan, Ann Arbor, MI 48109-1079, USA Abstract Questions about how shifting distributions contribute to species diversification remain virtually without answer, even though rapid climate change during the Pleistocene clearly impacted genetic variation within many species. One factor that has prevented this question from being adequately addressed is the lack of precision associated with estimates of species divergence made from a single genetic locus and without incorporating processes that are biologically important as populations diverge. Analysis of DNA sequences from multiple variable loci in a coalescent framework that (i) corrects for gene divergence pre-dating speciation, and (ii) derives divergence-time estimates without making a priori assumptions about the processes underlying patterns of incomplete lineage sorting between species (i.e. allows for the possibility of gene flow during speciation), is critical to overcoming the inherent logistical and analytical difficulties of inferring the timing and mode of speciation during the dynamic Pleistocene. Estimates of species divergence that ignore these processes, use single locus data, or do both can dramatically overestimate species divergence. For example, using a coalescent approach with data from six loci, the divergence between two species of montane Melanoplus grasshoppers is estimated at between 200 000 and 300 000 years before present, far more recently than divergence estimates made using single-locus data or without the incorporation of population-level processes. Melanoplus grasshoppers radiated in the sky islands of the Rocky Mountains, and the analysis of divergence between these species suggests that the isolation of populations in multiple glacial refugia was an important factor in promoting speciation. Furthermore, the low estimates of gene flow between the species indicate that reproductive isolation must have evolved rapidly for the incipient species boundaries to be maintained through the subsequent glacial periods and shifts in species distributions. Keywords: climate change, divergence time, glacial cycles, Pleistocene, speciation Received 5 September 2006; revision accepted 15 September 2006 difficulties with obtaining accurate divergence-time estimates Introduction if speciation was accompanied by gene flow. The periodicity The climatic cycles of the Pleistocene had a major impact of glacial cycles (Gates 1993) prevents glacial vs. interglacial on patterns of population genetic variation within many divergence, or divergence among different glacial periods, species (Hewitt 1996), yet it is unclear how these cycles from being distinguished without a precise estimate of the contributed to species diversification. This uncertainty reflects timing of speciation. Furthermore, with frequent distribu- the extreme difficulty of tracking species divergence during tional shifts in response to the glacial cycles (Pielou 1991; dynamic periods of climate change — not only is there a Elias 1996; Davis & Shaw 2001; Booth et al. 2004; Pierce challenge of obtaining sufficient genetic resolution for 2004; Thompson et al. 2004; Webb et al. 2004), there differentiating among hypotheses, but there are also analytical presumably would have been multiple opportunities for population isolation, but also gene flow given the lack of Correspondence: L. Lacey Knowles, Fax: (734) 763-4080; E-mail: long-term geographical barriers. When speciation does not [email protected] occur in strict allopatry (Wu 2001), estimates of divergence © 2006 The Authors Journal compilation © 2006 Blackwell Publishing Ltd 620 B. C. CARSTENS and L . L . KNOWLES will be appreciably underestimated when gene flow is lineage sorting between the species. Simulations under ignored (Nielsen & Wakeley 2001). conditions matching the empirical data set were then used The Pleistocene glacial cycles are thought to have played to determine whether this approach provided an accurate a central role in the formation of the 37 species of montane estimate of the timing of grasshopper speciation. These Melanoplus grasshoppers from the sky islands (or mountain simulations took into account the stochasticity of both tops) of the northern Rocky Mountains (Knowles 2000; mutational and lineage sorting processes, as well as varia- Knowles & Otte 2000). Patterns of widespread incomplete tion in mutation rates. This general approach (Knowles 2004; lineage sorting, and a largely unresolved polytomy in the Knowles & Maddison 2002) provides a framework for ask- species phylogeny, suggest that this diversity hot spot was ing whether the given data are adequate for estimating the generated by an explosive and recent radiation (Knowles timing of divergence under any specific historical scenario. 2001a). Two models have been proposed to explain Verifying that the empirical data can provide an accurate and how frequent and repeated climate-induced distributional precise divergence-time estimate is critical. Longstanding shifts might have promoted diversification in these grass- debate over the impact of the glacial cycles on species hoppers (Knowles 2001b). Speciation could have been diversity has been fuelled by divergence-time estimates initiated during (i) glacial periods by displacements with such broad confidence intervals that various claims into multiple refugia, or (ii) interglacials by the founding of about the effects of rapid climate change on species diver- the sky islands from ancestral glacial-source populations. gence during the dynamic Pleistocene cannot be rejected. Since the timing of species divergence is one of the key As yet, estimates of the timing of speciation have contributed components that allows these models to be differentiated, very little to our understanding of how shifting distributions and recognizing the difficulties with obtaining an accurate might have promoted speciation because of the logistical estimate of when divergence was initiated during periods and the analytical difficulties discussed below. of rapid climate change (Arbogast et al. 2002), we apply an integrative population genetic approach to examine how Methods Pleistocene distributional shifts might have contributed to species diversity. Sampling A multilocus approach was used to estimate the timing of divergence between two species, Melanoplus oregonensis Sequence data were collected from 21 individuals from and Melanoplus montanus; these taxa are members of the four Melanoplus oregonensis populations and 23 individuals diverse clade of montane grasshoppers that radiated in the from two Melanoplus montanus populations. Five anonymous northern Rocky Mountains (Knowles 2000). DNA sequences nuclear loci with an average length of 881 bp and 1147 bp from six variable loci (five anonymous nuclear markers of mitochondrial cytochrome oxidase I (COI) were sequenced identified from a genomic library and one mitochondrial (see Methods in Knowles 2001a). Across loci (a total of gene) were sequenced in more than 20 individuals for 5.5 kb) there were 409 variable sites, and three of the nuclear each species. A coalescent model that estimates ancestral loci contained indels (Table 1). The single-copy nuclear genetic diversity and incorporates a migration parameter polymorphic sequences (SCNPS) were identified from was used to estimate species divergence (Hey & Nielsen a genomic library using an interspecific screening set 2004), thereby allowing for the possibility of divergence that included a single representative from M. montanus, with gene flow and avoiding a priori assumptions about M. oregonensis, and Melanoplus marshalli, a closely related the processes underlying observed patterns of incomplete melanopline. The choice of loci was not based on levels Table 1 Genetic diversity statistics for each locus. From left to right, columns show the length of each locus in base pairs, the number of alleles, the number of insertion-deletions (with the length of the indels in parentheses), the number of polymorphic sites (s) excluding indels, and the nucleotide diversity (π) calculated by sites, the per-site theta calculated by migrate-n (θ) and its standard deviation, and Tajima’s D, with the P value calculated by simulation using arlequin Locus Length Alleles Indels s θ D COI 1147 36 0 125 0.0293 (0.023, 0.038) −0.320 P = 0.401 2 956 25 3 (31, 5, 19) 50 0.0104 (0.008, 0.017) −0.631 P = 0.304 73 853 18 0 10 0.007 (0.005, 0.013) 0.822 P = 0.962 85 826 41 0 58 0.0214 (0.009, 0.026) −1.412 P = 0.07 89 581 37 2 (11, 3) 51 0.0336 (0.028, 0.041) −0.216 P = 0.436 211 1188 30 4 (2, 4, 62, 7) 115 0.0146 (0.011, 0.024) 0.897 P = 0.765 © 2006 The Authors Journal compilation © 2006 Blackwell Publishing Ltd SHIFTING DISTRIBUTIONS AND SPECIATION 621 of variability within M. oregonensis or M. montanus (which distribution of parameter estimates was thoroughly inves- would introduce an ascertainment bias because the lower tigated. Since the data include five anonymous nuclear bound for allele frequencies would depend on the number loci with unknown mutation rates, the geometric mean of θ θ of individuals used to detect variable loci; Wakeley et al. the ratios i: COI for each of the five nuclear loci was used 2001). A plot of the distribution
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