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- NSF-PAR ID:
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- The American Naturalist
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Katz, Laura A (Ed.)Abstract Sterility among hybrids is one of the most prevalent forms of reproductive isolation delineating species boundaries and is expressed disproportionately in heterogametic XY males. While hybrid male sterility (HMS) due to the “large X effect” is a well-recognized mechanism of reproductive isolation, it is less clear how HMS manifests in species that lack heteromorphic sex chromosomes. We evaluated differences in allele frequencies at approximately 460,000 SNPs between fertile and sterile F2 interpopulation male hybrids to characterize the genomic architecture of HMS in a species without sex chromosomes (Tigriopus californicus). We tested associations between HMS and mitochondrial-nuclear and/or nuclear-nuclear signatures of incompatibility. Genomic regions associated with HMS were concentrated on a single chromosome with the same primary 2-Mbp regions identified in one pair of reciprocal crosses. Gene Ontology analysis revealed that annotations associated with spermatogenesis were the most overrepresented within the implicated region, with nine protein-coding genes connected with this process found in the quantitative trait locus of chromosome 2. Our results indicate that a narrow genomic region was associated with the sterility of male hybrids in T. californicus and suggest that incompatibilities among select nuclear loci may replace the large X effect when sex chromosomes are absent.more » « less
Abstract Reproductive isolation is the heuristic basis of the biological species concept, but what is it? Westram et al. (this issue) propose that it is a measurable quantity, “barrier strength,” that prevents gene flow among populations. However, their attempt to make the concept of reproductive isolation more scientific is unlikely to satisfy the diverse opinions of all evolutionary biologists. There are many different opinions about the nature of species, even under the biological species concept. Complete reproductive isolation, where gene flow is effectively zero, is regarded by some biologists as an important end point of speciation. Others, including Westram et al., argue for a more nuanced approach, and they also suggest that reproductive isolation may differ in different parts of the genome due to variation in genetic linkage to divergently selected loci. In contrast to both these approaches, we favour as a key criterion of speciation the stable coexistence of divergent populations in sympatry. Obviously, such populations must be reproductively isolated in some sense, but neither the fraction of the genome that is exchanged, nor measures of overall barrier strength acting on neutral variation will yield very precise predictions as to species status. Although an overall measure of reproductive isolation is virtually unattainable for these reasons, its early generation components, such as assortative mating, divergent selection, or hybrid inviability and sterility are readily measurable and remain informative. For example, we can make the prediction that to remain divergent in sympatry, almost all sexual species will require strong assortative mating, as well as some sort of ecological or intrinsic selection against hybrids and introgressed variants.more » « less
Postmating reproductive isolation can help maintain species boundaries when premating barriers to reproduction are incomplete. The strength and identity of postmating reproductive barriers are highly variable among diverging species, leading to questions about their genetic basis and evolutionary drivers. These questions have been tackled in model systems but are less often addressed with broader phylogenetic resolution. In this study we analyse patterns of genetic divergence alongside direct measures of postmating reproductive barriers in an overlooked group of sympatric species within the model monkeyflower genus,
Mimulus. Within this Mimulus brevipesspecies group, we find substantial divergence among species, including a cryptic genetic lineage. However, rampant gene discordance and ancient signals of introgression suggest a complex history of divergence. In addition, we find multiple strong postmating barriers, including postmating prezygotic isolation, hybrid seed inviability and hybrid male sterility. M. brevipesand M. fremontiihave substantial but incomplete postmating isolation. For all other tested species pairs, we find essentially complete postmating isolation. Hybrid seed inviability appears linked to differences in seed size, providing a window into possible developmental mechanisms underlying this reproductive barrier. While geographic proximity and incomplete mating isolation may have allowed gene flow within this group in the distant past, strong postmating reproductive barriers today have likely played a key role in preventing ongoing introgression. By producing foundational information about reproductive isolation and genomic divergence in this understudied group, we add new diversity and phylogenetic resolution to our understanding of the mechanisms of plant speciation.
Reproductive isolation between selfing and outcrossing species can arise through diverse mechanisms, some of which are directly associated with differences in mating system. We dissected cross-incompatibility between the highly selfing morning glory Ipomoea lacunosa and its mixed-mating sister species Ipomoea cordatotriloba. We found that cross-incompatibility is complex, with contributions acting both before and after fertilization. We then investigated whether the transition in mating system may have facilitated the evolution of these reproductive barrier components through mismatched floral morphology, differences in reproductive context, or both. We found evidence that morphological mismatch likely contributes to reproductive isolation in at least one cross-direction and that other pollen–pistil interactions are present. We also identified hybrid seed inviability consistent with the predictions of the weak-inbreeder, strong-outbreeder hypotheses, suggesting endosperm misregulation plays an important role in cross-incompatibility. In contrast, we did not find evidence consistent with the prezygotic weak-inbreeder, strong-outbreeder hypothesis. Our study highlights the complexity of reproductive isolation between outcrossing and selfing species and the extent to which evolutionary consequences of mating system transitions can facilitate speciation.
Incompatibilities on the sex chromosomes are important in the evolution of hybrid male sterility, but the evolutionary forces underlying this phenomenon are unclear. House mice (Mus musculus) lineages have provided powerful models for understanding the genetic basis of hybrid male sterility. X chromosome–autosome interactions cause strong incompatibilities in M. musculus F1 hybrids, but variation in sterility phenotypes suggests a more complex genetic basis. In addition, XY chromosome conflict has resulted in rapid expansions of ampliconic genes with dosage-dependent expression that is essential to spermatogenesis. Here, we evaluated the contribution of XY lineage mismatch to male fertility and stage-specific gene expression in hybrid mice. We performed backcrosses between two house mouse subspecies to generate reciprocal Y-introgression strains and used these strains to test the effects of XY mismatch in hybrids. Our transcriptome analyses of sorted spermatid cells revealed widespread overexpression of the X chromosome in sterile F1 hybrids independent of Y chromosome subspecies origin. Thus, postmeiotic overexpression of the X chromosome in sterile F1 mouse hybrids is likely a downstream consequence of disrupted meiotic X-inactivation rather than XY gene copy number imbalance. Y chromosome introgression did result in subfertility phenotypes and disrupted expression of several autosomal genes in mice with an otherwise nonhybrid genomic background, suggesting that Y-linked incompatibilities contribute to reproductive barriers, but likely not as a direct consequence of XY conflict. Collectively, these findings suggest that rapid sex chromosome gene family evolution driven by genomic conflict has not resulted in strong male reproductive barriers between these subspecies of house mice.