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1. Divergence of chemosensing during the early stages of speciation

   https://doi.org/10.1073/pnas.1921318117  

   van Schooten, Bas ; Meléndez-Rosa, Jesyka ; Van Belleghem, Steven M. ; Jiggins, Chris D. ; Tan, John D. ; McMillan, W. Owen ; Papa, Riccardo ( July 2020 , Proceedings of the National Academy of Sciences)

   Chemosensory communication is essential to insect biology, playing indispensable roles during mate-finding, foraging, and oviposition behaviors. These traits are particularly important during speciation, where chemical perception may serve to establish species barriers. However, identifying genes associated with such complex behavioral traits remains a significant challenge. Through a combination of transcriptomic and genomic approaches, we characterize the genetic architecture of chemoperception and the role of chemosensing during speciation for a young species pair of Heliconius butterflies, Heliconius melpomene and Heliconius cydno . We provide a detailed description of chemosensory gene-expression profiles as they relate to sensory tissue (antennae, legs, and mouthparts), sex (male and female), and life stage (unmated and mated female butterflies). Our results untangle the potential role of chemical communication in establishing barriers during speciation and identify strong candidate genes for mate and host plant choice behaviors. Of the 252 chemosensory genes, HmOBP20 (involved in volatile detection) and HmGr56 (a putative synephrine-related receptor) emerge as strong candidates for divergence in pheromone detection and host plant discrimination, respectively. These two genes are not physically linked to wing-color pattern loci or other genomic regions associated with visual mate preference. Altogether, our results provide evidence for chemosensory divergence between H. melpomene and H. cydno , two rarely hybridizing butterflies with distinct mate and host plant preferences, a finding that supports a polygenic architecture of species boundaries. 

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2. 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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3. A learning experience elicits sex‐dependent neurogenomic responses in Bicyclus anynana butterflies

   https://doi.org/10.1111/mec.16920  

   Ernst, David A. ; Agcaoili, Gabrielle A. ; Merrill, Abbigail N. ; Westerman, Erica L. ( March 2023 , Molecular Ecology)

   Sexually dimorphic behaviour is pervasive across animals, with males and females exhibiting different mate selection, parental care, foraging, dispersal, and territorial strategies. However, the genetic underpinnings of sexually dimorphic behaviours are poorly understood. Here we investigate gene networks and expression patterns associated with sexually dimorphic imprinting‐like learning in the butterflyBicyclus anynana. In this species, both males and females learn visual preferences, but learn preferences for different traits and use different signals as salient, unconditioned cues. To identify genes and gene networks associated with this behaviour, we examined gene expression profiles of the brains and eyes of male and female butterflies immediately post training and compared them to the same tissues of naïve individuals. We found more differentially expressed genes and a greater number of associated gene networks in the eyes, indicating a role of the peripheral nervous system in visual imprinting‐like learning. Females had higher chemoreceptor expression levels than males, supporting the hypothesized sexual dimorphic use of chemical cues during the learning process. In addition, genes that influenceB. anynanawing patterns (sexual ornaments), such asinvected,spalt, andapterous, were also differentially expressed in the brain and eye, suggesting that these genes may influence both sexual ornaments and the preferences for these ornaments. Our results indicate dynamic and sex‐specific responses to social scenario in both the peripheral and central nervous systems and highlight the potential role of wing patterning genes in mate preference and learning across the Lepidoptera.

    

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4. Response to MHC‐based olfactory cues in a mate choice context in two species of darter (Percidae: Etheostoma)

   https://doi.org/10.1002/ece3.11025  

   Million, Kara M. ; Proffit, Melissa R. ; Reese, Sierra J. ( February 2024 , Ecology and Evolution)

   Mate choice is hypothesized to play an important role in maintaining high diversity at major histocompatibility complex (MHC) genes in vertebrates. Many studies have revealed that females across taxa prefer the scent of males with MHC genotypes different to their own. In this study we tested the “opposites‐attract” hypothesis in two species of darter with known differences in female criteria used in mate choice: in the fantail darters (a paternal‐care species), females prefer males with visual traits related to nest guarding and egg tending, while in rainbow darters (not a paternal‐care species) female mate choice criteria are unknown. In dichotomous mate‐choice trials, we presented females of both species with the scents of conspecific males with MHC class IIb genotypes that were either similar or dissimilar to that of the focal female. We evaluated the proportion of time each female spent with each male and calculated the average strength of female preference for both species. Female fantail darters demonstrated a preference for the scent of males with similar (rather than dissimilar) MHC genotypes, but this result was not statistically significant. Rainbow darter females showed no preference for the scent of males with similar or dissimilar MHC genotypes. Our results do not support the “opposites‐attract” hypothesis in darters.

    

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5. Individual variation in preference behavior in sailfin fish refines the neurotranscriptomic pathway for mate preference

   https://doi.org/10.1002/ece3.10323  

   Young, Rebecca L. ; Price, Sarah M. ; Schumer, Molly ; Wang, Silu ; Cummings, Molly E. ( July 2023 , Ecology and Evolution)

   Social interactions can drive distinct gene expression profiles which may vary by social context. Here we use female sailfin molly fish (Poecilia latipinna) to identify genomic profiles associated with preference behavior in distinct social contexts: male interactions (mate choice) versus female interactions (shoaling partner preference). We measured the behavior of 15 females interacting in a non‐contact environment with either two males or two females for 30 min followed by whole‐brain transcriptomic profiling by RNA sequencing. We profiled females that exhibited high levels of social affiliation and great variation in preference behavior to identify an order of magnitude more differentially expressed genes associated with behavioral variation than by differences in social context. Using a linear model (limma), we took advantage of the individual variation in preference behavior to identify unique gene sets that exhibited distinct correlational patterns of expression with preference behavior in each social context. By combining limma and weighted gene co‐expression network analyses (WGCNA) approaches we identified a refined set of 401 genes robustly associated with mate preference that is independent of shoaling partner preference or general social affiliation. While our refined gene set confirmed neural plasticity pathways involvement in moderating female preference behavior, we also identified a significant proportion of discovered that our preference‐associated genes were enriched for ‘immune system’ gene ontology categories. We hypothesize that the association between mate preference and transcriptomic immune function is driven by the less well‐known role of these genes in neural plasticity which is likely involved in higher‐order learning and processing during mate choice decisions.

    

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