Which cues are sexy? The evolution of mate preference in sympatric species reveals the contrasted effect of adaptation and reproductive interference

Mate preferences may target traits (1) enhancing offspring adaptation and (2) reducing heterospecific matings. Because similar selective pressures are acting on traits shared by different sympatric species, preference enhancing offspring adaptation may increase heterospecific mating, in sharp contrast with the classical case of so-called ‘magic traits’. Using a mathematical model, we study which and how many traits will be used during mate choice, when preferences for locally adapted traits increase heterospecific mating. In particular, we study the evolution of preference towards an adaptive vs. a neutral trait in sympatric species. We take into account sensory trade-offs which may limit the emergence of preference for several traits. Our model highlights that the evolution of preference towards adaptive vs. neutral traits depends on the selective regimes acting on traits but also on heterospecific interactions. When the costs of heterospecific interactions are high, mate preference is likely to target neutral traits that become a reliable cue limiting heterospecific matings. We show that the evolution of preference towards a neutral trait benefits from a positive feedback loop: the more preference targets the neutral trait, the more it becomes a reliable cue for species recognition. We then reveal the key role of sensory trade-offs and the cost of choosiness favouring the evolution of preferences targeting adaptive traits, rather than traits reducing heterospecific mating. When sensory trade-offs and the cost of choosiness are low, we also show that preferences targeting multiple traits evolve, improving offspring fitness by both transmitting adapted alleles and reducing heterospecific mating. Altogether, our model aims at reconciling ‘good gene’ and reinforcement models to provide general predictions on the evolution of mate preferences within natural communities. Impact Summary Mate preferences are widespread throughout the animal kingdom and generate powerful selective forces impacting the diversification of traits and species. The evolution of such preferences has been the focus of multiple theoretical and empirical studies and intense scientific debates. The evolution of mate preference (1) enhancing offspring fitness and (2) reducing heterospecific mating have been mostly studied separately, except in the specific case of preference for so-called ‘magic traits’ that increase both offspring survival and species divergence. However, in many cases, the evolution of traits in sympatric species generates conflicting evolutionary forces acting on preferences. On one hand, enhanced offspring survival promotes preference towards locally adaptive traits and may thus lead to convergent evolution of traits among sympatric species. On the other hand, the evolution of similar traits in sympatric species may generate costly heterospecific sexual interactions promoting preference towards traits that diverge between species. Here, we thus build a general mathematical model to investigate the evolutionary factors determining which and how many traits are targeted by mate choice. We especially determine whether preferences will likely target adaptive vs. neutral traits. Our model highlights that the evolution of preferences for adaptive vs. neutral traits in sympatric species depends on within-species mating opportunities but also on the niche overlap between species, tuning heterospecific interactions. By jointly considering (1) the selection regimes acting on the targeted traits within species, as well as (2) interactions with other species living in sympatry, our theoretical study provides a general framework reconciling these research fields.