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Epistatic interactions between loci that reduce fitness in interspecies hybrids, Dobzhansky–Muller incompatibilities (DMIs), contribute genetically to the inviability and infertility within hybrid populations. It remains a challenge, however, to identify the loci that contribute to DMIs as causes of reproductive isolation between species. Here, we assess through forward simulation the power of evolve‐and‐resequence (E&R) experimental evolution of hybrid populations to map DMI loci. We document conditions under which such a mapping strategy may be most feasible and demonstrate how mapping power is sensitive to biologically relevant parameters such as one‐way versus two‐way incompatibility type, selection strength, recombination rate, and dominance interactions. We also assess the influence of parameters under direct control of an experimenter, including duration of experimental evolution and number of replicate populations. We conclude that an E&R strategy for mapping DMI loci, and other cases of epistasis, can be a viable option under some circumstances for study systems with short generation times like Caenorhabditis nematodes. [ABSTRACT FROM AUTHOR]

Ontogenetic development hinges on the changes in gene expression in time and space within an organism, suggesting that the demands of ontogenetic growth can impose or reveal predictable pattern in the molecular evolution of genes expressed dynamically across development. Here, we characterize coexpression modules of the Caenorhabditis elegans transcriptome, using a time series of 30 points from early embryo to adult. By capturing the functional form of expression profiles with quantitative metrics, we find fastest evolution in the distinctive set of genes with transcript abundance that declines through development from a peak in young embryos. These genes are highly enriched for oogenic function and transient early zygotic expression, are nonrandomly distributed in the genome, and correspond to a life stage especially prone to inviability in interspecies hybrids. These observations conflict with the "early conservation model" for the evolution of development, although expression‐weighted sequence divergence analysis provides some support for the "hourglass model." Genes in coexpression modules that peak toward adulthood also evolve fast, being hyper‐enriched for roles in spermatogenesis, implicating a history of sexual selection and relaxation of selection on sperm as key factors driving rapid change to ontogenetically distinguishable coexpression modules of genes. We propose that these predictable trends of molecular evolution for dynamically expressed genes across ontogeny predispose particular life stages, early embryogenesis in particular, to hybrid dysfunction in the speciation process. [ABSTRACT FROM AUTHOR]

Speciation genetics research in diverse organisms shows the X‐chromosome to be exceptional in how it contributes to "rules" of speciation. Until recently, however, the nematode phylum has been nearly silent on this issue, despite the model organism Caenorhabditis elegans having touched most other topics in biology. Studies of speciation with Caenorhabditis accelerated with the recent discovery of species pairs showing partial interfertility. The resulting genetic analyses of reproductive isolation in nematodes demonstrate key roles for the X‐chromosome in hybrid male sterility and inviability, opening up new understanding of the genetic causes of Haldane's rule, Darwin's corollary to Haldane's rule, and enabling tests of the large‐X effect hypothesis. Studies to date implicate improper chromatin regulation of the X‐chromosome by small RNA pathways as integral to hybrid male dysfunction. Sexual transitions in reproductive mode to self‐fertilizing hermaphroditism inject distinctive molecular evolutionary features into the speciation process for some species. Caenorhabditis also provides unique opportunities for analysis in a system with XO sex determination that lacks a Y‐chromosome, sex chromosome‐dependent sperm competition differences and mechanisms of gametic isolation, exceptional accessibility to the development process and rapid experimental evolution. As genetic analysis of reproductive isolation matures with investigation of multiple pairs of Caenorhabditis species and new species discovery, nematodes will provide a powerful complement to more established study organisms for deciphering the genetic basis of and rules to speciation. [ABSTRACT FROM AUTHOR]

The richness of biodiversity in the tropics compared to high-latitude parts of the world forms one of the most globally conspicuous patterns in biology, and yet few hypotheses aim to explain this phenomenon in terms of explicit microevolutionary mechanisms of speciation and extinction. We link population genetic processes of selection and adaptation to speciation and extinction by way of their interaction with environmental factors to drive global scale macroecological patterns. High-latitude regions are both cradle and grave with respect to species diversification. In particular, we point to a conceptual equivalence of 'environmental harshness' and 'hard selection' as eco-evolutionary drivers of local adaptation and ecological speciation. By describing how ecological speciation likely occurs more readily at high latitudes, with such nascent species especially prone to extinction by fusion, we derive the ephemeral ecological speciation hypothesis as an integrative mechanistic explanation for latitudinal gradients in species turnover and the net accumulation of biodiversity. [ABSTRACT FROM AUTHOR]

Recent research has filled many gaps about Caenorhabditis natural history, simultaneously exposing how much remains to be discovered. This awareness now provides means of connecting ecological and evolutionary theory with diverse biological patterns within and among species in terms of adaptation, sexual selection, breeding systems, speciation, and other phenomena. Moreover, the heralded laboratory tractability of C. elegans, and Caenorhabditis species generally, provides a powerful case study for experimental hypothesis testing about evolutionary and ecological processes to levels of detail unparalleled by most study systems. Here, I synthesize pertinent theory with what we know and suspect about Caenorhabditis natural history for salient features of biodiversity, phenotypes, population dynamics, and interactions within and between species. I identify topics of pressing concern to advance Caenorhabditis biology and to study general evolutionary processes, including the key opportunities to tackle problems in dispersal dynamics, competition, and the dimensionality of niche space. [ABSTRACT FROM AUTHOR]

Highlights: [•] Phylogenomics and population genomics set a new standard of analysis in molecular evolution. [•] Evolutionary theory and genomic data can help bridge population processes to macroevolution. [•] Genome structural features can predictably affect gene tree heterogeneity. [•] I discuss theoretical and empirical complexities, solutions, and ways to exploit genomic structure. [•] Integrative molecular evolution improves understanding of biodiversity at all levels. [ABSTRACT FROM AUTHOR]

The genomic density of sequence polymorphisms critically affects the sensitivity of inferences about ongoing sequence evolution, function and demographic history. Most animal and plant genomes have relatively low densities of polymorphisms, but some species are hyperdiverse with neutral nucleotide heterozygosity exceeding 5%. Eukaryotes with extremely large populations, mimicking bacterial and viral populations, present novel opportunities for studying molecular evolution in sexually reproducing taxa with complex development. In particular, hyperdiverse species can help answer controversial questions about the evolution of genome complexity, the limits of natural selection, modes of adaptation and subtleties of the mutation process. However, such systems have some inherent complications and here we identify topics in need of theoretical developments. Close relatives of the model organisms Caenorhabditis elegans and Drosophila melanogaster provide known examples of hyperdiverse eukaryotes, encouraging functional dissection of resulting molecular evolutionary patterns. We recommend how best to exploit hyperdiverse populations for analysis, for example, in quantifying the impact of noncrossover recombination in genomes and for determining the identity and micro-evolutionary selective pressures on noncoding regulatory elements. [ABSTRACT FROM AUTHOR]

Everyone appreciates the happy fiction that species conform to the simple theoretical convenience of a single panmictic population. In speciation genetics, a further standard simplification is that it is only those genetic differences that are fixed between diverging populations that need concern us in order to understand the accumulation of intrinsic barriers to reproduction. To a first approximation, of course, both of these assumptions are appropriate and theory based on them provides compelling insights into diverse evolutionary phenomena (Orr & Turelli ). But what else can we learn about the begetting of biodiversity, speciation, by considering explicitly some less convenient realities of natural populations? Specifically, how does genetic variation at incompatibility loci within a species influence interspecies hybridization upon secondary contact? And, in nature, how repeatable among distinct bouts of secondary contact are the genomic outcomes of hybridization? Mandeville et al. () tackle exactly this question in their new study in Molecular Ecology on five species of suckers, fish of the genus Catostomus, that overlap sympatrically in different portions of their subdivided ranges that occupy different rivers. They document substantial genomic heterogeneity in realized hybridization in nature, both among species pairs and among the source populations for hybrids of a given species pair. This imperfect repeatability of episodes of hybridization implies greater permeability of species barriers in some parts of their range, with intriguing consequences for how the integrity of species as independently evolving units could be susceptible to collapse. [ABSTRACT FROM AUTHOR]

Deciphering the genetic and developmental causes of the disproportionate rarity, inviability, and sterility of hybrid males, Haldane's rule, is important for understanding the evolution of reproductive isolation between species. Moreover, extrinsic and prezygotic factors can contribute to the magnitude of intrinsic isolation experienced between species with partial reproductive compatibility. Here, we use the nematodes Caenorhabditis briggsae and C. nigoni to quantify the sensitivity of hybrid male viability to extrinsic temperature and developmental timing, and test for a role of mito-nuclear incompatibility as a genetic cause. We demonstrate that hybrid male inviability manifests almost entirely as embryonic, not larval, arrest and is maximal at the lowest rearing temperatures, indicating an intrinsic-by-extrinsic interaction to hybrid inviability. Crosses using mitochondrial substitution strains that have reciprocally introgressed mitochondrial and nuclear genomes show that mito-nuclear incompatibility is not a dominant contributor to postzygotic isolation and does not drive Haldane's rule in this system. Crosses also reveal that competitive superiority of X-bearing sperm provides a novel means by which postmating prezygotic factors exacerbate the rarity of hybrid males. These findings highlight the important roles of gametic, developmental, and extrinsic factors in modulating the manifestation of Haldane's rule. [ABSTRACT FROM AUTHOR]

Sperm from other species invade female tissues to cause sterility and death, helping to keep nematode species boundaries intact. [ABSTRACT FROM AUTHOR]

The process of speciation is key to the origins of biodiversity, and yet the Caenorhabditis nematode model system has contributed little to this topic. Genetic studies of speciation in the genus are now feasible, owing to crosses between the recently discovered Caenorhabditis sp. 9 and the well-known C. briggsae producing fertile F1 hybrid females. We dissected patterns of postzygotic reproductive isolation between these species by crossing eight isogenic strains of C. briggsae reciprocally with six strains of C. sp. 9. We determined that overall patterns of reproductive isolation are robust across these genetic backgrounds. However, we also quantified significant heritable variation within each species for interspecific hybrid incompatibilities for total adult progeny, egg-to-adult viability, and the percentage of male progeny. This demonstrates that intraspecific variation for interspecific hybrid incompatibility occurs despite extensive, albeit incomplete, reproductive isolation. Therefore, this emerging general phenomenon of variable reproductive isolation is not restricted to highly interfertile, early-stage incipient species, but also applies to species in the latest stages of the speciation process. Furthermore, we confirm Haldane's rule and demonstrate strongly asymmetric parent-of-origin effects (Darwin's corollary) that consistently manifest more extremely when hermaphroditic C. briggsae serves as maternal parent. These findings highlight Caenorhabditis as an emerging system for understanding the genetics of general patterns of reproductive isolation. [ABSTRACT FROM AUTHOR]