Understanding the origins and mechanisms of biological diversity is a fundamental question for biologists. Visible traits such as colour patterns are classically used to study the mechanisms that promote diversity because colour patterns are amenable to ecological research and their roles are often well characterised. In that context, the existence of local variation in colour patterns used as warning signals is a long-standing enigma because natural selection is expected to promote signal uniformity and erase diversity. Warning signals are used by toxic prey to advertise their unprofitability. Predators can use these signals to learn to avoid such prey, and in turn prey reduce the chances of being eaten. When a certain warning signal is common, prey bearing that signal are more likely to encounter predators that have already learnt to avoid it, generating a positive link between the frequency of the signal and the survival protection it confers (positive frequency-dependent selection). Since the most common signal is favoured, this type of selection regime erodes phenotypic diversity by promoting trait fixation within populations. However, warning signal diversity can occasionally be observed within populations. A classic example is the spectacular variation of the Amazonian butterfly Heliconius numata. This toxic species always displays multiple colour patterns within populations, with up to seven distinct ‘morphs’ coexisting in a given locality. Recent work has shown that warning signal variation can be maintained through sexual selection, which can have strong effects opposing natural selection and act as a powerful source of diversification. For example, if individuals prefer mates with phenotypes distinct from their own (disassortative mating), the rarer phenotypes will benefit from a higher availability of mates and attain higher reproductive success, which will counter the tendency of signal fixation. Indeed, contrary to all other species of Heliconius studied so far, H. numata exhibits disassortative mating patterns. Despite a key role of mate preferences as a powerful agent of sexual selection that maintains warning signal variation in the face of opposing natural selection, how disassortative mate choice is encoded and expressed remains an open question.
Females may use different sensory modalities to evaluate potential mates and will typically prefer males that possess certain traits – what Darwin termed female’s ‘standard of beauty’. Well-studied examples include female preferences for conspicuous colour signals, complex songs, or for males with colour and/or chemical patterns that resemble their own (i.e. assortative mating). Despite considerable knowledge on female preferences linked to the evolution of male ornaments or with regards to assortative mating, the mechanisms underlying disassortative mate preferences are far less understood. The exception is arguably work on disassortative mating based on major histocompatibility complex (MHC), showing that mammals and fish have odour-based preference for partners with dissimilar or complementary sets of MHC alleles. However, the potential role of complementary multimodal cues in disassortative mating preferences has not yet been examined, despite its importance for uncovering the genetic basis of disassortative mate preference.
Recent theoretical work suggests that disassortative mating is more likely to evolve by genes coding for self-referencing or rejection linked to the genes for wing colour, compared to preference genes. While the expected mate preference of females if the genes code for self-referencing or rejection will be similar, complicating our ability of inferring which mechanism exists, it will depend on the strength of the linkage between rejection and wing colour alleles. In contrast, preference alleles may generate preference for two different wing types in males that have different copies of the genes, and therefore not always result in rejection of similar males. I will experimentally test these predictions by measuring female rejection behaviour towards males of varying genotypes and examining the link between wing colour genotype, observable pattern, and female choice.
To further muddy the waters, female choice may not be under complete genetic control. Since rejecting males can be costly (because choosy females spend time and energy looking for the best male), mate choice decisions are often modulated by experience and/or the female’s ability to incur such costs. Yet, the extent to which females modulate mate choice decisions in the context of disassortative mating remains untested.
Unravelling these questions constitutes a promising line of research that will shed light on the behavioural mechanisms maintaining disassortative mate preferences and contribute invaluable and exciting insights that will pave the ground for future research. The occurrence of disassortative mating in H. numata is an evolutionary paradox that remains poorly understood. This project aims to capitalize on the well-characterized Heliconius system to examine the behavioural mechanisms involved in disassortative mate choice in H. numata.
It will provide high-quality new knowledge on disassortative mating that extends to several disciplines (animal behaviour and cognition, evolution, genetics, and animal communication) and will have long-term implications since it will stimulate new ideas and further research on mate choice and warning signal evolution. This project will also strengthen human capital in Research & Innovation (R&I) by reinforcing my position as an excellent researcher, as well as through the transfer of knowledge from me to host institution researchers and students I will mentor.
