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1. Conflict over fertilization underlies the transient evolution of reinforcement

   https://doi.org/10.1371/journal.pbio.3001814  

   Rushworth, Catherine A. ; Wardlaw, Alison M. ; Ross-Ibarra, Jeffrey ; Brandvain, Yaniv ( October 2022 , PLOS Biology)

   Jennions, Michael D. (Ed.)

   When two species meet in secondary contact, the production of low fitness hybrids may be prevented by the adaptive evolution of increased prezygotic isolation, a process known as reinforcement. Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem, i.e., “how can statistical associations between traits and preferences be maintained in the face of recombination?” However, the evolution of reinforcement also poses a potential conflict between mates. For example, the opportunity costs to hybridization may differ between the sexes or species. This is particularly likely for reinforcement based on postmating prezygotic (PMPZ) incompatibilities, as the ability to fertilize both conspecific and heterospecific eggs is beneficial to male gametes, but heterospecific mating may incur a cost for female gametes. We develop a population genetic model of interspecific conflict over reinforcement inspired by “gametophytic factors”, which act as PMPZ barriers among Zea mays subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement—after females adaptively evolve to reject gametes lacking a signal common in conspecific gametes, this gamete signal adaptively introgresses into the other population. Ultimately, the male gamete signal fixes in both species, and isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among Z . mays subspecies considering these findings and suggest when and how this conflict can be resolved. Our results suggest that sexual conflict over fertilization may pose an understudied obstacle to the evolution of reinforcement. 

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2. The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers

   https://doi.org/10.1111/jeb.13495  

   Larson, Erica L. ; Brassil, Margaret M. ; Maslan, Jonathan ; Juárez, Danielle ; Lilagan, Flordeliza ; Tipton, Hallie ; Schweitzer, Andrew ; Skillman, Joe ; Monsen‐Collar, Kirsten J. ; Peterson, Merrill A. ( June 2019 , Journal of Evolutionary Biology)

   Heterospecific mating frequency is critical to hybrid zone dynamics and can directly impact the strength of reproductive barriers and patterns of introgression. The effectiveness of post‐mating prezygotic (PMPZ) reproductive barriers, which include reduced fecundity via heterospecific matings and conspecific sperm precedence, may depend on the number, identity and order of mates. Studies ofPMPZbarriers suggest that they may be important in many systems, but whether these barriers are effective at realistic heterospecific mating frequencies has not been tested. Here, we evaluate the strength of cryptic reproductive isolation in two leaf beetles (Chrysochus auratusandC. cobaltinus) in the context of a range of heterospecific mating frequencies observed in natural populations. We found both species benefited from multiple matings, but the benefits were greater inC. cobaltinusand extended to heterospecific matings. We found thatPMPZbarriers greatly limited hybrid production byC. auratusfemales with moderate heterospecific mating frequencies, but that their effectiveness diminished at higher heterospecific mating frequencies. In contrast, there was no evidence forPMPZbarriers inC. cobaltinusfemales at any heterospecific mating frequency. We show that integrating realistic estimates of cryptic isolation with information on relative abundance and heterospecific mating frequency in the field substantially improves our understanding of the strong directional bias in F1 production previously documented in theChrysochushybrid zone. Our results demonstrate that heterospecific mating frequency is critical to understanding the impact of cryptic post‐copulatory barriers on hybrid zone structure and dynamics, and that future studies of such barriers should incorporate field‐relevant heterospecific mating frequencies.

    

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3. Strong postmating reproductive isolation in Mimulus section Eunanus

   https://doi.org/10.1111/jeb.14219  

   Farnitano, Matthew C. ; Sweigart, Andrea L. ( September 2023 , Journal of Evolutionary Biology)

   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 thisMimulus 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. brevipesandM. 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.

    

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4. Molecular mechanisms of postmating prezygotic reproductive isolation uncovered by transcriptome analysis

   https://doi.org/10.1111/mec.13679  

   Pease, James B. ; Guerrero, Rafael F. ; Sherman, Natasha A. ; Hahn, Matthew W. ; Moyle, Leonie C. ( May 2016 , Molecular Ecology)

   Little is known about the physiological responses and genetic mutations associated with reproductive isolation between species, especially for postmating prezygotic isolating barriers. Here, we examine changes in gene expression that accompany the expression of ‘unilateral incompatibility’ (UI)—a postmating prezygotic barrier in which fertilization is prevented by gamete rejection in the reproductive tract [in this case of pollen tubes (male gametophytes)] in one direction of a species cross, but is successful in the reciprocal crossing direction. We use whole‐transcriptome sequencing of multiple developmental stages of male and female tissues in twoSolanumspecies that exhibitUIto: (i) identify transcript differences betweenUI‐competent andUInoncompetent tissues; (ii) characterize transcriptional changes specifically associated with the phenotypic expression ofUI; and (iii) using these comparisons, evaluate the behaviour of a priori candidate loci forUIand identify new candidates for future manipulative work. In addition to describing transcriptome‐wide changes in gene expression that accompany this isolating barrier, we identify at least five strong candidates for involvement in postmating prezygotic incompatibility between species. These include three novel candidates and two candidates that are strongly supported by prior developmental, functional, and quantitative trait locus mapping studies. These latter genes are known molecular players in the intraspecific expression of mate choice via genetic self‐incompatibility, and our study supports prior evidence that these inter‐ and intraspecific postmating prezygotic reproductive behaviours share specific genetic and molecular mechanisms.

    

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5. Molecular Diversification of the Seminal Fluid Proteome in a Recently Diverged Passerine Species Pair

   https://doi.org/10.1093/molbev/msz235  

   Rowe, Melissah ; Whittington, Emma ; Borziak, Kirill ; Ravinet, Mark ; Eroukhmanoff, Fabrice ; Sætre, Glenn-Peter ; Dorus, Steve ; Larracuente, Amanda ( October 2019 , Molecular Biology and Evolution)

   Abstract Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows. 

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