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  1. Explaining broad molecular, phenotypic and species biodiversity patterns necessitates a unifying framework spanning multiple evolutionary scales. Here we argue that although substantial effort has been made to reconcile microevolution and macroevolution, much work remains to identify the links between biological processes at play. We highlight four major questions of evolutionary biology whose solutions require conceptual bridges between micro and macroevolution. We review potential avenues for future research to establish how mechanisms at one scale (drift, mutation, migration, selection) translate to processes at the other scale (speciation, extinction, biogeographic dispersal) and vice versa. We propose ways in which current comparative methods to infer molecular evolution, phenotypic evolution and species diversification could be improved to specifically address these questions. We conclude that researchers are in a better position than ever before to build a synthesis to understand how microevolutionary dynamics unfold over millions of years. 
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    Free, publicly-accessible full text available August 1, 2024
  2. Abstract

    The role of hybridization in diversification is complex and may result in many possible outcomes. Not only can hybridization produce new lineages, but those lineages may contain unique combinations of adaptive genetic variation derived from parental taxa that allow hybrid‐origin lineages to occupy unique environmental space relative to one (or both) parent(s). We document such a case of hybridization between two sedge species,Carex novaandCarex nelsonii(Cyperaceae), that occupy partially overlapping environmental space in the southern Rocky Mountains, USA. In the region hypothesized to be the origin of the hybrid lineage, one parental taxon (C. nelsonii) is at the edge of its environmental tolerance. Hybrid‐origin individuals display mixed ancestry between the parental taxa—of nearly 7000 unlinked loci sampled, almost 30% showed evidence of excess ancestry from one parental lineage—approximately half displayed a genomic background skewed towards one parent, and half skewed towards the other. To test whether excess ancestry loci may have conferred an adaptive advantage to the hybrid‐origin lineage, we conducted genotype–environment association analyses on different combinations of loci—with and without excess ancestry—and with multiple contrasts between the hybrids and parental taxa. Loci with skewed ancestry showed significant environmental associations distinguishing the hybrid lineage from one parent (C. nelsonii), whereas loci with relatively equal representation of parental ancestries showed no such environmental associations. Moreover, the overwhelming majority of candidate adaptive loci with respect to environmental gradients also had excess ancestry from a parental lineage, implying these loci have facilitated the persistence of the hybrid lineage in an environment unsuitable to at least one parent.

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  3. Abstract

    Assessments of spatial and temporal congruency across taxa from genetic data provide insights into the extent to which similar processes structure communities. However, for coastal regions that are affected continuously by cyclical sea‐level changes over the Pleistocene, congruent interspecific response will not only depend upon codistributions, but also on similar dispersal histories among taxa. Here, we use SNPs to test for concordant genetic structure among four codistributed taxa of freshwater fishes (Teleostei: Characidae) along the Brazilian Atlantic coastal drainages. Based on population relationships and hierarchical genetic structure analyses, we identify all taxa share the same geographic structure suggesting the fish utilized common passages in the past to move between river basins. In contrast to this strong spatial concordance, model‐based estimates of divergence times indicate that despite common routes for dispersal, these passages were traversed by each of the taxa at different times resulting in varying degrees of genetic differentiation across barriers with most divergences dating to the Upper Pleistocene, even when accounting for divergence with gene flow. Interestingly, when this temporal dissonance is viewed through the lens of the species‐specific ecologies, it suggests that an ecological sieve influenced whether species dispersed readily, with an ecological generalist showing the highest propensity for historical dispersal among the isolated rivers of the Brazilian coast (i.e., the most recent divergence times and frequent gene flow estimated for barriers). We discuss how our findings, and in particular what the temporal dissonance, despite common geographic passages, suggest about past dispersal structuring coastal communities as a function of ecological and paleo‐landscape sieves.

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  4. Abstract

    Rapid speciation events, with taxa generated over a short time period, are among the most investigated biological phenomena. However, molecular systematics often reveals contradictory results compared with morphological/phenotypical diagnoses of species under scenarios of recent and rapid diversification. In this study, we used molecular data from an average of over 29 000 loci per sample from RADseq to reconstruct the diversification history and delimit the species boundary in a short‐winged grasshopper species complex (Melanoplus scudderigroup), where Pleistocene diversification has been hypothesized to generate more than 20 putative species with distinct male genitalic shapes. We found that, based on a maximum likelihood molecular phylogeny, each morphological species indeed forms a monophyletic group, contrary to the result from a previous mitochondrial DNA sequence study. By dating the diversification events, the species complex is estimated to have diversified during the Late Pleistocene, supporting the recent radiation hypothesis. Furthermore, coalescent‐based species delimitation analyses provide quantitative support for independent genetic lineages, which corresponds to the morphologically defined species. Our results also showed that male genitalic shape may not be predicted by evolutionary distance among species, not only indicating that this trait is labile, but also implying that selection may play a role in character divergence. Additionally, our findings suggest that the rapid speciation events in this flightless grasshopper complex might be primarily associated with the fragmentation of their grassland habitats during the Late Pleistocene. Collectively, our study highlights the importance of integrating multiple sources of information to delineate species, especially for a species complex that diversified rapidly, and whose divergence may be linked to ecological processes that create geographic isolation (i.e. fragmented habitats), as well as selection acting on characters with direct consequences for reproductive isolation (i.e. genitalic divergence).

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  5. Abstract

    Museum genomics has transformed the field of collections‐based research, opening up a range of new research directions for paleontological specimens as well as natural history specimens collected over the past few centuries. Recent work demonstrates that it is possible to characterize epigenetic markers such as DNA methylation in well preserved ancient tissues. This approach has not yet been tested in traditionally prepared natural history specimens such as dried bones and skins, the most common specimen types in vertebrate collections. In this study, we developed and tested methods to characterize cytosine methylation in dried skulls up to 76 years old. Using a combination of ddRAD and bisulphite treatment, we characterized patterns of cytosine methylation in two species of deer mouse (Peromyscusspp.) collected in the same region in Michigan in 1940, 2003, and 2013–2016. We successfully estimated methylation in specimens of all age groups, although older specimens yielded less data and showed greater interindividual variation in data yield than newer specimens. Global methylation estimates were reduced in the oldest specimens (76 years old) relative to the newest specimens (1–3 years old), which may reflect post‐mortem hydrolytic deamination. Methylation was reduced in promoter regions relative to gene bodies and showed greater bimodality in autosomes relative to female X chromosomes, consistent with expectations for methylation in mammalian somatic cells. Our work demonstrates the utility of historic specimens for methylation analyses, as with genomic analyses; however, studies will need to accommodate the large variance in the quantity of data produced by older specimens.

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  6. Abstract

    Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genusPheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus,Pheidoleworkers are evolving as a mixture of intracaste and intercaste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.

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