Genomic tests of the species‐pump hypothesis: Recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/111904/1/evo12667-sup-0001-SuppMat.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/111904/2/evo12667.pd

Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation

Determining what factors affect the structuring of genetic variation is key to deciphering the relative roles of different evolutionary processes in species differentiation. Such information is especially critical to understanding how the frequent shifts and fragmentation of species distributions during the Pleistocene translates into species differences, and why the effect of such rapid climate change on patterns of species diversity varies among taxa. Studies of mitochondrial DNA (mtDNA) have detected significant population structure in many species, including those directly impacted by the glacial cycles. Yet, understanding the ultimate consequence of such structure, as it relates to how species divergence occurs, requires demonstration that such patterns are also shared with genomic patterns of differentiation. Here we present analyses of amplified fragment length polymorphisms (AFLPs) in the montane grasshopper Melanoplus oregonensis to assess the evolutionary significance of past demographic events and associated drift-induced divergence as inferred from mtDNA. As an inhabitant of the sky islands of the northern Rocky Mountains, this species was subject to repeated and frequent shifts in species distribution in response to the many glacial cycles. Nevertheless, significant genetic structuring of M . oregonensis is evident at two different geographic and temporal scales: recent divergence associated with the recolonization of the montane meadows in individual sky islands, as well as older divergence associated with displacements into regional glacial refugia. The genomic analyses indicate that drift-induced divergence, despite the lack of long-standing geographic barriers, has significantly contributed to species divergence during the Pleistocene. Moreover, the finding that divergence associated with past demographic events involves the repartitioning of ancestral variation without significant reductions of genomic diversity has intriguing implications — namely, the further amplification of drift-induced divergence by selection.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/75590/1/j.1365-294X.2005.02711.x.pd

Recombination rate and protein evolution in yeast

<p>Abstract</p> <p>Background</p> <p>Theory and artificial selection experiments show that recombination can promote adaptation by enhancing the efficacy of natural selection, but the extent to which recombination affects levels of adaptation across the genome is still an open question. Because patterns of molecular evolution reflect long-term processes of mutation and selection in nature, interactions between recombination rate and genetic differentiation between species can be used to test the benefits of recombination. However, this approach faces a major difficulty: different evolutionary processes (i.e. negative versus positive selection) produce opposing relationships between recombination rate and genetic divergence, and obscure patterns predicted by individual benefits of recombination.</p> <p>Results</p> <p>We use a combination of polymorphism and genomic data from the yeast <it>Saccharomyces cerevisiae </it>to infer the relative importance of nearly-neutral (i.e. slightly deleterious) evolution in different gene categories. For genes with high opportunities for slightly deleterious substitution, recombination substantially reduces the rate of molecular evolution, whereas divergence in genes with little opportunity for slightly deleterious substitution is not strongly affected by recombination.</p> <p>Conclusion</p> <p>These patterns indicate that adaptation throughout the genome can be strongly influenced by each gene's recombinational environment, and suggest substantial long-term fitness benefits of enhanced purifying selection associated with sexual recombination.</p

Tests of phenotypic and genetic concordance and their application to the conservation of Panamanian golden frogs (Anura, Bufonidae)

Evolutionarily significant units (ESUs) differ in the extent to which they capture, or even consider, adaptive variation, and most such designations are based solely on neutral genetic differences that may not capture variation relevant to species’ adaptabilities to changing environmental conditions. While concordant patterns of divergence among data sets (i.e. neutral and potentially non‐neutral characters) can strengthen ESU designations, determining whether such criteria are met for highly variable taxa is especially challenging. This study tests whether previously defined ESUs for endangered Panamanian golden frogs ( Atelopus varius and Atelopus zeteki ) exhibit concordant variation among multiple phenotypic traits and mitochondrial DNA sequences, and the extent to which such divergence corresponds to environmental differences. Multivariate analyses identify phenotypic and genetic differentiation consistent with proposed ESUs and support the status of A. varius and A. zeteki as separate species. Moreover, the significant association detected between ESU co‐membership and genetic similarity, which remained strong after removing the effect of geographic distance, also indicates that genetic differences are not simply due to isolation by distance. Two phenotypic characters (body size and the extent of dorsal black patterning) that differ among ESUs also co‐vary with environmental differences, suggesting that to the extent that these phenotypic differences are heritable, variation may be associated with adaptive divergence. Lastly, discriminant function analyses show that the frogs can be correctly assigned to ESUs based on simultaneous analysis of multiple characters. The study confirms the merit of conserving the previously proposed golden frog ESUs as well as demonstrates the utility and feasibility of combined analyses of ecological, morphological and genetic variation in evaluating ESUs, especially for highly variable taxa.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/102716/1/j.1365-294X.2007.03369.x.pd

Species‐specific responses to island connectivity cycles: refined models for testing phylogeographic concordance across a Mediterranean Pleistocene Aggregate Island Complex

The contribution of Pleistocene sea level changes to diversification patterns in archipelagos around the world, and specifically whether the repeated cycles of island connectivity and isolation acted as a ‘species pump’ is debated. The debate has been perpetuated in part because of the type of evidence used to evaluate the species‐pump hypothesis. Specifically, existing tests of the ‘Pleistocene Aggregate Island Complex’ (PAIC) model of diversification interpret the lack of concordant divergence times among multiple codistributed taxa as a rejection of the PAIC model. However, the null expectation of concordance disregards taxon‐specific ecological traits and geographic characteristics that may affect population persistence and gene flow among islands. Here, we study the factors affecting population divergence in thirteen flightless darkling beetle species (Coleoptera: Tenebrionidae) across the PAIC system of the Cycladic plateau in the Aegean archipelago. Based on isolation‐by‐resistance analyses, hierarchical amova and the degree of genealogical sorting on individual islands, we identify a major effect of bathymetry and habitat stability on the levels of genetic divergence across the PAIC, with island size and body size playing a secondary role as well. We subsequently use bathymetric maps and habitat association to generate predictions about the set of islands and group of taxa expected to show phylogeographic concordance. We test these predictions using hierarchical approximate Bayesian computation and show how our interpretations regarding the role of PAICs as drivers of divergence change when relying on a null expectation of concordance compared to a refined model that takes geography and ecological traits into account.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/113138/1/mec13305.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/113138/2/mec13305_am.pd

Navigating the unknown: model selection in phylogeography

Despite the widespread use and obvious strengths of model-based methods for phylogeographic study, a persistent concern for such analyses is related to the definition of the model itself. The study by Peter et al. (2010) in this issue of Molecular Ecology demonstrates an approach for overcoming such hurdles. The authors were motivated by a deceptively simple goal; they sought to infer whether a population has remained at a low and stable size or has undergone a decline, and certainly there is no shortage of software packages for such a task (e.g., see list of programs in Excoffier & Heckel 2006 ). However, each of these software packages makes basic assumptions about the underling population (e.g., is the population subdivided or panmictic); these assumptions are explicit to any model-based approach but can bias parameter estimates and produce misleading inferences if the model does not approximate the actual demographic history in a reasonable manner. Rather than guessing which model might be best for analyzing the data (microsatellite data from samples of chimpanzees), Peter et al. (2010) quantify the relative fit of competing models for estimating the population genetic parameters of interest. Complemented by a revealing simulation study, the authors highlight the peril inherent to model-based inferences that lack a statistical evaluation of the fit of a model to the data, while also demonstrating an approach for model selection with broad applicability to phylogeographic analysis.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/79081/1/j.1365-294X.2010.04851.x.pd

Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence

Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/72231/1/j.1365-294X.2009.04305.x.pd

Shifting distributions and speciation: species divergence during rapid climate change

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.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/75592/1/j.1365-294X.2006.03167.x.pd

Exploring the population genetic consequences of the colonization process with spatio-temporally explicit models: insights from coupled ecological, demographic and genetic models in montane grasshoppers

Understanding the genetic consequences of shifting species distributions is critical for evaluating the impact of climate-induced distributional changes. However, the demographic expansion associated with the colonization process typically takes place across a heterogeneous environment, with population sizes and migration rates varying across the landscape. Here we describe an approach for coupling ecological-niche models (ENMs) with demographic and genetic models to explore the genetic consequences of distributional shifts across a heterogeneous landscape. Analyses of a flightless grasshopper from the sky islands of the Rocky Mountains of North America are used to show how biologically informed predictions can be generated about the genetic consequences of a colonization process across a spatially and temporally heterogeneous landscape (i.e. the suitability of habitats for the montane species differs across the landscape and is itself not static, with the displacement of contemporary populations into glacial refugia). By using (i) ENMs for current climatic conditions and the last glacial maximum to (ii) parameterize a demographic model of the colonization process, which then (iii) informs coalescent simulations, a set of models can be generated that capture different processes associated with distributional shifts. We discuss how the proposed approach for model generation can be integrated into a statistical framework for estimating key demographic parameters and testing hypotheses about the conditions for which distributional shifts may (or may not) enhance species divergence, including the importance of habitat stability, past gene-flow among currently isolated populations, and maintenance of refugial populations in multiple geographic regions.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/79315/1/MEC_4702_sm_Supplemental-Tables.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/79315/2/j.1365-294X.2010.04702.x.pd

Testing for biogeographic mechanisms promoting divergence in Caribbean crickets (genus Amphiacusta )

This work examines whether the history of diversification of Amphiacusta (Orthoptera, Gryllidae) in the Caribbean corresponds to a vicariant or a dispersalist model.The Greater Antillean islands of the Caribbean region.The phylogenetic relationships among species were estimated using a procedure that directly estimates the underlying species tree from independent loci (in this case, one mitochondrial and one nuclear locus). This tree was then used to test for topological congruence with a vicariant model, and to estimate divergence times.The analyses based on the expected pattern of species divergence (i.e. species-tree topology) support a vicariant model. With the notable exception of a dispersal event marking the colonization of Jamaica, the timing of the events are generally consistent with a vicariant scenario, given the current taxon sampling and potential errors with dating the divergence events.The tendency of species to co-segregate by island suggests that intra-island diversification is common. Despite their flightlessness, species of Amphiacusta are apparently capable of long-distance dispersal, such as colonization from the Puerto Rican/Virgin Island bank to Jamaica. The topology of the species tree is consistent with a vicariant model of divergence, and the dates of divergence between island groups are generally consistent with an island–island vicariance model. A strict island–island vicariance scenario can, however, be rejected because of inferred dispersal events such as the colonization of Jamaica. Nevertheless, the biogeographic tests suggest that most of the diversity was generated under a combination of intra-island diversification and island–island vicariance. Additional sampling of taxa will be needed to verify this hypothesized scenario. Our findings indicate that Amphiacusta presents an ideal opportunity for examining the role of sexual selection in promoting diversification, which would complement the large number of studies focused on adaptive divergence of Caribbean taxa.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/79301/1/j.1365-2699.2009.02231.x.pd