Molecular basis and evolution of visual mate recognition in Heliconius butterflies
Evolution, Anthropology
Final Report Abstract
Many closely related animal species remain separate not because they fail to produce viable offspring, but because they effectively ‘choose’ not to do so in the first place. Although the significance of behavioural barriers for speciation has been recognized since the early 20th century, we know little of the genes underlying changes in mating preferences, or variation in behaviours across natural populations more broadly. Our project concerns behavioural preferences for visual mating cues. Animals often use colour, and other visual cues, to attract and recognize suitable mates. The evolution of these colour cues is increasingly understood at the genetic level, but the genes underlying variation in the corresponding preferences remain unknown. This is significant because identifying the genes involved is key to uncovering how behavioural variation is generated during development, and across evolutionary time. We studied tropical Heliconius butterflies, which display a diversity of bright warning patterns. These warning patterns are also used during mate choice, and we have endeavoured to identify the genetic basis of variation in preference behaviours in relation to that of the corresponding colour pattern cues. Combining extensive behavioural experiments with genomic analyses and CRISPR/Cas9 techniques we have made a number of important discoveries relating to the evolution and genetic basis of visual preferences. Most significantly, we have identified – for the first time in any animal – a major gene underlying visual preference behaviour. This work makes three important and novel contributions: We identify and functionally test a behavioural gene in Heliconius, representing a significant empirical advance and shedding light on how complex behaviours can be encoded within the genome. We resolve the genetic identity of tightly linked loci underlying local adaptation and assortative mating, addressing long-standing questions in speciation research. We provide the first direct link between a specific behaviour and a specific introgressed gene, showing that hybridization between species can drive behavioural evolution. Overall, our results allow us to more fully appreciate the co-evolutionary history of genes underlying both cue and preference responsible for population divergence and the evolution of new species. Moreover, it opens doors to the next step of understanding how the brain integrates visual stimuli and translates genetic changes into divergent ecologically relevant behaviours.
Publications
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Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates. Journal of Evolutionary Biology, 26(7), 1499-1507.
Leclaire, S.; Nielsen, J. F.; Sharp, S. P. & Clutton‐Brock, T. H.
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The biology of color. Science, 357(6350).
Cuthill, Innes C.; Allen, William L.; Arbuckle, Kevin; Caspers, Barbara; Chaplin, George; Hauber, Mark E.; Hill, Geoffrey E.; Jablonski, Nina G.; Jiggins, Chris D.; Kelber, Almut; Mappes, Johanna; Marshall, Justin; Merrill, Richard; Osorio, Daniel; Prum, Richard; Roberts, Nicholas W.; Roulin, Alexandre; Rowland, Hannah M.; Sherratt, Thomas N. ... & Caro, Tim
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Genetic dissection of assortative mating behavior. PLOS Biology, 17(2), e2005902.
Merrill, Richard M.; Rastas, Pasi; Martin, Simon H.; Melo, Maria C.; Barker, Sarah; Davey, John; McMillan, W. Owen & Jiggins, Chris D.
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Visual mate preference evolution during butterfly speciation is linked to neural processing genes. Nature Communications, 11(1).
Rossi, Matteo; Hausmann, Alexander E.; Thurman, Timothy J.; Montgomery, Stephen H.; Papa, Riccardo; Jiggins, Chris D.; McMillan, W. Owen & Merrill, Richard M.
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Light environment influences mating behaviours during the early stages of divergence in tropical butterflies. Proceedings of the Royal Society B: Biological Sciences, 288.
Hausmann, Alexander E.; Kuo, Chi-Yun; Freire, Marília; Rueda-M, Nicol; Linares, Mauricio; Pardo-Diaz, Carolina; Salazar, Camilo & Merrill, Richard M.
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Neural divergence and hybrid disruption between ecologically isolatedHeliconiusbutterflies. Proceedings of the National Academy of Sciences, 118(6).
Montgomery, Stephen H.; Rossi, Matteo; McMillan, W. Owen & Merrill, Richard M.
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Evolution of physical linkage between loci controlling ecological traits and mating preferences. Journal of Evolutionary Biology, 35(11), 1537-1547.
Schuldiner‐Harpaz, Tarryn; Merrill, Richard M. & Jiggins, Chris D.
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Adaptive introgression of a visual preference gene.
Rossi, Matteo; Hausmann, Alexander E.; Alcami, Pepe; Moest, Markus; Wright, Daniel Shane; Kuo, Chi-Yun; Lozano, Daniela; Maulana, Arif; Melo-Flórez, Lina; Muñoz, Geraldine Rueda-; McMahon, Saoirse; Linares, Mauricio; Owen, McMillan W.; Pardo-Diaz, Carolina; Salazar, Camilo & Merrill, Richard M.
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Frizzled2 receives WntA signaling during butterfly wing pattern formation. Development, 150(18).
Hanly, Joseph J.; Loh, Ling S.; Mazo-Vargas, Anyi; Rivera-Miranda, Teomie S.; Livraghi, Luca; Tendolkar, Amruta; Day, Christopher R.; Liutikaite, Neringa; Earls, Emily A.; Corning, Olaf B. W. H.; D'Souza, Natalie; Hermina-Perez, José J.; Mehta, Caroline; Ainsworth, Julia A.; Rossi, Matteo; Papa, Riccardo; McMillan, W. Owen; Perry, Michael W. & Martin, Arnaud
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Genetics and the Evolution of Prezygotic Isolation. Cold Spring Harbor Perspectives in Biology, 16(2), a041439.
Merrill, Richard M.; Arenas-Castro, Henry; Feller, Anna F.; Harenčár, Julia; Rossi, Matteo; Streisfeld, Matthew A. & Kay, Kathleen M.
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Divergent warning patterns influence male and female mating behaviours in a tropical butterfly. Journal of Evolutionary Biology, 37(3), 267-273.
Kuo, Chi-Yun; Melo-Flóres, Lina; Aragón, Andrea; Oberweiser, Morgan M.; McMillan, W. Owen; Pardo-Diaz, Carolina; Salazar, Camilo & Merrill, Richard M.
