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1. Strong postmating reproductive isolation in Mimulus section Eunanus

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

   Farnitano, Matthew C. ; Sweigart, Andrea L. ( October 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 this Mimulus brevipes species 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. brevipes and M. fremontii have 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.

   Abstract

   Hybrid seed inviability and other postmating reproductive barriers isolate species in Mimulus section Eunanus. Variation in seed size may help explain hybrid seed failure. Whole-genome sequencing indicates a complex history of divergence, including signals of ancient introgression and cryptic diversity.

    

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2. A genetic switch for male UV iridescence in an incipient species pair of sulphur butterflies

   https://doi.org/10.1073/pnas.2109255118  

   Ficarrotta, Vincent ; Hanly, Joseph J. ; Loh, Ling S. ; Francescutti, Caroline M. ; Ren, Anna ; Tunström, Kalle ; Wheat, Christopher W. ; Porter, Adam H. ; Counterman, Brian A. ; Martin, Arnaud ( January 2022 , Proceedings of the National Academy of Sciences)

   Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of ultraviolet (UV) iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern United States with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis- regulatory variation of bric a brac ( bab ) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knockout, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation. 

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3. Diet‐based assortative mating through sexual imprinting

   https://doi.org/10.1002/ece3.5630  

   Delaney, Emily K. ; Hoekstra, Hopi E. ( September 2019 , Ecology and Evolution)

   Speciation is facilitated by “magic traits,” where divergent natural selection on such traits also results in assortative mating. In animal populations, diet has the potential to act as a magic trait if populations diverge in consumed food that incidentally affects mating and therefore sexual isolation. While diet‐based assortative mating has been observed in the laboratory and in natural populations, the mechanisms causing positive diet‐based assortment remain largely unknown. Here, we experimentally created divergent diets in a sexually imprinting species of mouse,Peromyscus gossypinus(the cotton mouse), to test the hypothesis that sexual imprinting on diet could be a mechanism that generates rapid and significant sexual isolation. We provided breeding pairs with novel garlic‐ or orange‐flavored water and assessed whether their offspring, exposed to these flavors in utero and in the nest before weaning, later preferred mates that consumed the same flavored water as their parents. While males showed no preference, females preferred males of their parental diet, which is predicted to yield moderate sexual isolation. Thus, our experiment demonstrates the potential for sexual imprinting on dietary cues learned in utero and/or postnatally to facilitate reproductive isolation and potentially speciation.

   This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available athttps://doi.org/10.5061/dryad.n1qq6v3.

    

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4. Female mate choice is a reproductive isolating barrier in Heliconius butterflies

   https://doi.org/10.1111/eth.12818  

   Southcott, Laura ; Kronforst, Marcus R. ; Bertram, ed., S. ( November 2018 , Ethology)

   In sexually reproducing organisms, speciation involves the evolution of reproductive isolating mechanisms that decrease gene flow. Premating reproductive isolation, often the result of mate choice, is a major obstacle to gene flow between species because it acts earlier in the life cycle than other isolating barriers. While female choice is often considered the default mode in animal species, research in the butterfly genusHeliconius, a frequent subject of speciation studies, has focused on male mate choice.We studied mate choice byHeliconius cydnofemales by pairing them with either conspecific males or males of the closely related speciesHeliconius pachinus. Significantly more intraspecific trials than interspecific trials resulted in mating. Because male courtship rates did not differ between the species when we excluded males that never courted, we attribute this difference to female choice. Females also performed more acceptance behaviours towards conspecific males. Premating isolation between these two species thus entails both male and female mate choice, and female choice may be an important factor in the origin ofHeliconiusspecies.

    

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5. Sexual signal evolution and patterns of assortative mating across an intraspecific contact zone

   https://doi.org/10.1111/jeb.14186  

   Pascal, Florine J. M. ; Vega, Andrés ; Akopyan, Maria ; Hoke, Kim L. ; Robertson, Jeanne M. ( June 2023 , Journal of Evolutionary Biology)

   Contact zones provide important insights into the evolutionary processes that underlie lineage divergence and speciation. Here, we use a contact zone to ascertain speciation potential in the red‐eyed treefrog (Agalychnis callidryas), a brightly coloured and polymorphic frog that exhibits unusually high levels of intraspecific variation. Populations ofA. callidryasdiffer in a number of traits, several of which are known sexual signals that mediate premating reproductive isolation in allopatric populations. Along the Caribbean coast of Costa Rica, a ~100 km contact zone, situated between two phenotypically and genetically divergent parent populations, contains multiple colour pattern phenotypes and late‐generation hybrids. This contact zone provides the opportunity to examine processes that are important in the earliest stages of lineage divergence. We performed analyses of colour pattern variation in five contact zone sites and six parental sites and found complex, continuous colour variation along the contact zone. We found discordance between the geographic distribution of colour pattern and previously described genomic population structure. We then used a parental site and contact zone site to measure assortative mating and directional selection from naturally‐occurring amplectant mating pairs. We found assortative mating in a parental population, but no assortative mating in the contact zone. Furthermore, we uncovered evidence of directional preference towards the adjacent parental phenotype in the contact zone population, but no directional preference in the parent population. Combined, these data provide insights into potential dynamics at the contact zone borders and indicate that incipient speciation between parent populations will be slowed.

    

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