Abstract Influential models of speciation by sexual selection posit either a single shared preference for a universal display, expressed only when males are locally adapted and hence in high condition, or that shared loci evolve population‐specific alleles for displays and preferences. However, many closely related species instead show substantial differences across categorically different traits. We present a model of secondary contact whereby females maintain preferences for distinct displays that indicate both male condition and their match to distinct environments, fostering reproductive isolation among diverging species. This occurs even with search costs and with independent preference loci targeting independent displays. Such preferences can also evolve from standing variation. Divergence occurs because condition‐dependent display and female preference depend on local ecology, and females obtain different benefits of choice. Given the ubiquity of ecological differences among environments, our model could help explain the evolution of striking radiations of displays seen in nature.
more »
« less
The Fisher process of sexual selection with the coevolution of preference strength
Abstract Sexual selection has a rich history of mathematical models that consider why preferences favor one trait phenotype over another (for population genetic models) or what specific trait value is preferred (for quantitative genetic models). Less common is exploration of the evolution of choosiness or preference strength: i.e., by how much a trait is preferred. We examine both population and quantitative genetic models of the evolution of preferences, specifically developing “baseline models” of the evolution of preference strength during the Fisher process. Using a population genetic approach, we find selection for stronger and stronger preferences when trait variation is maintained by mutation. However, this force is quite weak and likely to be swamped by drift in moderately-sized populations. In a quantitative genetic model, unimodal preferences will generally not evolve to be increasingly strong without bounds when male traits are under stabilizing viability selection, but evolve to extreme values when viability selection is directional. Our results highlight that different shapes of fitness and preference functions lead to qualitatively different trajectories for preference strength evolution ranging from no evolution to extreme evolution of preference strength.
more »
« less
- Award ID(s):
- 1939290
- PAR ID:
- 10404534
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution
- Volume:
- 77
- Issue:
- 4
- ISSN:
- 0014-3820
- Format(s):
- Medium: X Size: p. 1043-1055
- Size(s):
- p. 1043-1055
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Patricelli, Gail L. (Ed.)Sexual selection by mate choice is a powerful force that can lead to evolutionary change, and models of why females choose particular mates are central to understanding its effects. Predominant mate choice theories assume preferences are determined solely by genetic inheritance, an assumption still lacking widespread support. Moreover, preferences often vary among individuals or populations, fail to correspond with conspicuous male traits, or change with context, patterns not predicted by dominant models. Here, we propose a new model that explains this mate choice complexity with one general hypothesized mechanism, “Inferred Attractiveness.” In this model, females acquire mating preferences by observing others’ choices and use context-dependent information to infer which traits are attractive. They learn to prefer the feature of a chosen male that most distinguishes him from other available males. Over generations, this process produces repeated population-level switches in preference and maintains male trait variation. When viability selection is strong, Inferred Attractiveness produces population-wide adaptive preferences superficially resembling “good genes.” However, it results in widespread preference variation or nonadaptive preferences under other predictable circumstances. By casting the female brain as the central selective agent, Inferred Attractiveness captures novel and dynamic aspects of sexual selection and reconciles inconsistencies between mate choice theory and observed behavior.more » « less
-
Males in many species have elaborated sexual traits that females strongly prefer, and these traits often conspicuously differ among species. How novel preferences and traits originate, however, is a challenging evolutionary problem because the initial appearance of only the female preference or only the male trait should reduce the ability to find a suitable mate, which could reduce fitness for individuals possessing those novel alleles. Here, we present a hypothesis for how novel preferences, as well as the novel male traits that females prefer, can originate, be favoured and spread in polyandrous species. Novel preference mutations can arise as ‘veiled preferences’ that are not expressed when the corresponding male trait is not present in the population, allowing preferences to be hidden from selection, and thus persist. In those cases when a male trait is present, veiled preferences provide a selective advantage, and females disproportionately produce offspring from preferred males through either mate choice or cryptic female choice. This tips the fitness advantage for novel males, allowing both preference and trait to spread, and limiting selection against them in the absence of the corresponding trait or preference.more » « less
-
Upon the secondary contact of populations, speciation with gene flow is greatly facilitated when the same pleiotropic loci are both subject to divergent ecological selection and induce non-random mating, leading to loci with this fortuitous combination of functions being referred to as ‘magic trait’ loci. We use a population genetics model to examine whether ‘pseudomagic trait’ complexes, composed of physically linked loci fulfilling these two functions, are as efficient in promoting premating isolation as magic traits. We specifically measure the evolution of choosiness, which controls the strength of assortative mating. We show that, surprisingly, pseudomagic trait complexes, and to a lesser extent also physically unlinked loci, can lead to the evolution of considerably stronger assortative mating preferences than do magic traits, provided polymorphism at the involved loci is maintained. This is because assortative mating preferences are generally favoured when there is a risk of producing maladapted recombinants, as occurs with non-magic trait complexes but not with magic traits (since pleiotropy precludes recombination). Contrary to current belief, magic traits may not be the most effective genetic architecture for promoting strong premating isolation. Therefore, distinguishing between magic traits and pseudomagic trait complexes is important when inferring their role in premating isolation. This calls for further fine-scale genomic research on speciation genes.more » « less
-
Abstract In contrast to sexual selection on traits that affect interactions between the sexes before mating, little theoretical research has focused on the coevolution of postmating traits via cryptic female choice (when females bias fertilization toward specific males). We used simulation models to ask (a) whether and, if so, how nondirectional cryptic female choice (female-by-male interactions in fertilization success) causes deviations from models that focus exclusively on male-mediated postmating processes, and (b) how the risk of sperm competition, the strength of cryptic female choice, and tradeoffs between sperm number and sperm traits interact to influence the coevolutionary dynamics between cryptic female choice and sperm traits. We found that incorporating cryptic female choice can result in males investing much less in their ejaculates than predicted by models with sperm competition only. We also found that cryptic female choice resulted in the evolution of genetic correlations between cryptic female choice and sperm traits, even when the strength of cryptic female choice was weak, and the risk of sperm competition was low. This suggests that cryptic female choice may be important even in systems with low multiple mating. These genetic correlations increased with the risk of sperm competition and as the strength of cryptic female choice increased. When the strength of cryptic female choice and risk of sperm competition was high, extreme codivergence of sperm traits and cryptic female choice preference occurred even when the sperm trait traded off with sperm number. We also found that male traits lagged behind the evolution of female traits; this lag decreased with increasing strength of cryptic female choice and risk of sperm competition. Overall, our results suggest that cryptic female choice deserves more attention theoretically and may be driving trait evolution in ways just beginning to be explored.more » « less
An official website of the United States government
