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Hybridization is an evolutionary phenomenon that has fascinated biologists for centuries. Prior to the advent of whole-genome sequencing, it was clear that hybridization had played a role in the evolutionary history of many extant taxa, particularly plants. The extent to which hybridization has contributed to the evolution of Earth’s biodiversity has, however, been the topic of much debate. Analyses of whole genomes are providing further insight into this evolutionary problem. Recent studies have documented ancient hybridization in a diverse array of taxa including mammals, birds, fish, fungi, and insects. Evidence for adaptive introgression is being documented in an increasing number of systems, though demonstrating the adaptive function of introgressed genomic regions remains difficult. And finally, several new homoploid hybrid speciation events have been reported. Here we review the current state of the field and specifically evaluate the additional insights gained from having access to whole-genome data and the challenges that remain with respect to understanding the evolutionary relevance and frequency of ancient hybridization, adaptive introgression, and hybrid speciation in nature. This Review discusses recent advances in our understanding of the evolutionary importance of ancient hybridization, adaptive introgression, and hybrid speciation brought about by whole genome data of non-model organisms.

One of the central questions in evolutionary genetics is how much of the genome is involved in the early stages of divergence between populations, causing them to be reproductively isolated. In this article, we investigate genomic differentiation in a pair of closely related field crickets (Gryllus firmus and G. pennsylvanicus). These two species are the result of allopatric divergence and now interact along an extensive hybrid zone in eastern North America. Genes encoding seminal fluid proteins (SFPs) are often divergent between species, and it has been hypothesized that these proteins may play a key role in the origin and maintenance of reproductive isolation between diverging lineages. Hence, we chose to scan the accessory gland transcriptome to enable direct comparisons of differentiation for genes known to encode SFPs with differentiation in a much larger set of genes expressed in the same tissue. We have characterized differences in allele frequency between two populations for >6000 SNPs and >26,000 contigs. About 10% of all SNPs showed nearly fixed differences between the two species. Genes encoding SFPs did not have significantly elevated numbers of fixed SNPs per contig, nor did they seem to show larger differences than expected in their average allele frequencies. The distribution of allele frequency differences across the transcriptome is distinctly bimodal, but the relatively high proportion of fixed SNPs does not necessarily imply “ancient” divergence between these two lineages. Further studies of linkage disequilibrium and introgression across the hybrid zone are needed to direct our attention to those genome regions that are important for reproductive isolation.

Hybrid sterility is a complex phenotype that can result from the breakdown of spermatogenesis at multiple developmental stages. Here, we disentangle two proposed hybrid male sterility mechanisms in the house mice, Mus musculus domesticus and M. m. musculus, by comparing patterns of gene expression in sterile F1 hybrids from a reciprocal cross. We found that hybrid males from both cross directions showed disrupted X chromosome expression during prophase of meiosis I consistent with a loss of meiotic sex chromosome inactivation (MSCI) and Prdm9-associated sterility, but that the degree of disruption was greater in mice with an M. m. musculus X chromosome consistent with previous studies. During postmeiotic development, gene expression on the X chromosome was only disrupted in one cross direction, suggesting that misexpression at this later stage was genotype-specific and not a simple downstream consequence of MSCI disruption which was observed in both reciprocal crosses. Instead, disrupted postmeiotic expression may depend on the magnitude of earlier disrupted MSCI, or the disruption of particular X-linked genes or gene networks. Alternatively, only hybrids with a potential deficit of Sly copies, a Y-linked ampliconic gene family, showed overexpression in postmeiotic cells, consistent with a previously proposed model of antagonistic coevolution between the X- and Y-linked ampliconic genes contributing to disrupted expression late in spermatogenesis. The relative contributions of these two regulatory mechanisms and their impact on sterility phenotypes await further study. Our results further support the hypothesis that X-linked hybrid sterility in house mice has a variable genetic basis, and that genotype-specific disruption of gene regulation contributes to overexpression of the X chromosome at different stages of development. Overall, these findings underscore the critical role of epigenetic regulation of the X chromosome during spermatogenesis and suggest that these processes are prone to disruption in hybrids.

The theory and practice of evolutionary tree-thinking is pervasive through many scientific fields and is a critical component of biological literacy. Many elements of tree-thinking are introduced early in undergraduate biology education. However, basic concepts are often not revisited/reinforced and are assumed to have been fully conceptually grasped in upper-level courses and beyond. Here, we present a project-based activity that we developed to aid upper-level biology students to learn, conceptualize, and practice tree-thinking. This approach allows them to identify the misconceptions that they may have about tree-thinking, while reinforcing the theories and concepts that they may have encountered in introductory courses. It also integrates several pedagogical styles (instructor-led and student-centered), along with an organismal case study to make concepts concrete and realistic to students.

Orthopterans are commonly encountered in rural, suburban, and urban landscapes and have charismatic songs that attract the public’s attention. These are ideal organisms for connecting the public with science and critical concepts in ecology and evolution, such as habitat conservation and climate change. In this review, we provide an overview of community science and review community science in orthopterans. Best practices for orthopteran community science are provided, with a focus on audio recordings and highlighting new ways in which scientists who study orthopterans can engage in community science. Before the modern era, scientific discovery was commonly made by people who were not scientists by profession (Brenna 2011, Miller-Rushing et al. 2012). This began to change in the middle of the nineteenth century when science became highly academic, with greater “gatekeeping” of knowledge, and data collection became increasingly expensive. As a result, much of the knowledge gained during that time has been effectively withheld from non-scientists in difficult-to-obtain scientific journals, and there were few opportunities for the public to directly engage with scientific research. In recent years, there has been a concerted effort from the scientific community to change the way we engage with the public. These “citizen” or “community” science projects are filling gaps in the modern approach to scientific inquiry (Jordan et al. 2012, Toomey and Domroese 2013, Johnson et al. 2014). Here, we provide an overview of community science and highlight the exciting and unique role that community science can play in orthopteran research. We focus on how acoustic surveys can be used to study orthopteran biodiversity, provide best practices for orthopteran community science, and suggest future avenues for research.

Patterns of morphological divergence across species’ ranges can provide insight into local adaptation and speciation. In this study, we compared phenotypic divergence among 4,221 crickets from 337 populations of two closely related species of field cricket, Gryllus firmus and G. pennsylvanicus, and their hybrids. We found that these species differ across their geographic range in key morphological traits, such as body size and ovipositor length, and we directly compared phenotype with genotype for a subset of crickets to demonstrate nuclear genetic introgression, phenotypic intermediacy of hybrids, and essentially unidirectional mitochondrial introgression. We discuss how these morphological traits relate to life history differences between the two species. Our comparisons across geographic areas support prior research suggesting that cryptic variation within G. firmus may represent different species. Our study highlights how variable morphology can be across wide-ranging species and the importance of studying reproductive barriers in more than one or two transects of a hybrid zone.

Whole tissue RNASeq is the standard approach for studying gene expression divergence in evolutionary biology and provides a snapshot of the comprehensive transcriptome for a given tissue. However, whole tissues consist of diverse cell types differing in expression profiles, and the cellular composition of these tissues can evolve across species. Here, we investigate the effects of different cellular composition on whole tissue expression profiles. We compared gene expression from whole testes and enriched spermatogenesis populations in two species of house mice, Mus musculus musculus and M. m. domesticus, and their sterile and fertile F1 hybrids, which differ in both cellular composition and regulatory dynamics. We found that cellular composition differences skewed expression profiles and differential gene expression in whole testes samples. Importantly, both approaches were able to detect large-scale patterns such as disrupted X chromosome expression, although whole testes sampling resulted in decreased power to detect differentially expressed genes. We encourage researchers to account for histology in RNASeq and consider methods that reduce sample complexity whenever feasible. Ultimately, we show that differences in cellular composition between tissues can modify expression profiles, potentially altering inferred gene ontological processes, insights into gene network evolution, and processes governing gene expression evolution.

Post-copulatory interactions between males and females involve highly coordinated, complex traits that are often rapidly evolving and divergent between species. Failure to produce and deposit eggs may be a common post-mating prezygotic barrier, yet little is known about what prevents the induction of egg-laying between species. The field crickets, Gryllus firmus and G. pennsylvanicus are isolated by a one-way reproductive incompatibility; G. pennsylvanicus males fail to fertilize G. firmus eggs or to induce normal egg-laying in G. firmus females. We use experimental crosses to elucidate the role of accessory gland-derived vs. testis-derived components of the G. firmus male ejaculate on egg-laying in conspecific and heterospecific crosses. Using surgical castrations to create 'spermless' males that transfer only seminal fluid proteins (SFPs) we test whether G. firmus male SFPs can induce egg-laying in conspecific crosses and rescue egg-laying in crosses between G. pennsylvanicus males and G. firmus females. We find G. firmus SFPs induce only a small short-term egg-laying response and that SFPs alone cannot explain the normal induction of egg-laying. Gryllus firmus SFPs also do not rescue the heterospecific cross. Testis-derived components, such as sperm or prostaglandins, most likely stimulate egg-laying or act as transporters for SFPs to targets in the female reproductive tract. These results highlight the utility of experimental approaches for investigating the phenotypes that act as barriers between species and suggest that future work on the molecular basis of the one-way incompatibility between G. firmus and G. pennsylvanicus should focus on divergent testis-derived compounds or proteins in addition to SFPs.

Abstract Genes involved in spermatogenesis tend to evolve rapidly, but we lack a clear understanding of how protein sequences and patterns of gene expression evolve across this complex developmental process. We used fluorescence-activated cell sorting (FACS) to generate expression data for early (meiotic) and late (postmeiotic) cell types across 13 inbred strains of mice (Mus) spanning ∼7 My of evolution. We used these comparative developmental data to investigate the evolution of lineage-specific expression, protein-coding sequences, and expression levels. We found increased lineage specificity and more rapid protein-coding and expression divergence during late spermatogenesis, suggesting that signatures of rapid testis molecular evolution are punctuated across sperm development. Despite strong overall developmental parallels in these components of molecular evolution, protein and expression divergences were only weakly correlated across genes. We detected more rapid protein evolution on the X chromosome relative to the autosomes, whereas X-linked gene expression tended to be relatively more conserved likely reflecting chromosome-specific regulatory constraints. Using allele-specific FACS expression data from crosses between four strains, we found that the relative contributions of different regulatory mechanisms also differed between cell types. Genes showing cis-regulatory changes were more common late in spermatogenesis, and tended to be associated with larger differences in expression levels and greater expression divergence between species. In contrast, genes with trans-acting changes were more common early and tended to be more conserved across species. Our findings advance understanding of gene evolution across spermatogenesis and underscore the fundamental importance of developmental context in molecular evolutionary studies.

The disruption of meiotic sex chromosome inactivation (MSCI) has been proposed to be a major developmental mechanism underlying the rapid evolution of hybrid male sterility. We tested this idea by analyzing cell-specific gene expression across spermatogenesis in two lineages of house mice and their sterile and fertile reciprocal hybrids. We found pervasive disruption of sex chromosome gene expression in sterile hybrids at every stage of spermatogenesis. Failure of MSCI was developmentally preceded by increased silencing of autosomal genes, supporting the hypothesis that divergence at the hybrid incompatibility gene, Prdm9, results in increased rates of autosomal asynapsis which in turn triggers widespread silencing of unsynapsed chromatin. We also detected opposite patterns of postmeiotic overexpression or hyper-repression of the sex chromosomes in reciprocal hybrids, supporting the hypothesis that genomic conflict has driven functional divergence that leads to deleterious X–Y dosage imbalances in hybrids. Our developmental timeline also exposed more subtle patterns of mitotic misregulation on the X chromosome, a previously undocumented stage of spermatogenic disruption in this cross. These results indicate that multiple hybrid incompatibilities have converged on a common regulatory phenotype, the disrupted expression of the sex chromosomes during spermatogenesis. Collectively, these data reveal a composite regulatory basis to hybrid male sterility in mice that helps resolve the mechanistic underpinnings of the well-documented large X-effect in mice speciation. We propose that the inherent sensitivity of spermatogenesis to X-linked regulatory disruption has the potential to be a major driver of reproductive isolation in species with chromosomal sex determination.