scholarly journals Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects

2006 ◽  
Vol 273 (1601) ◽  
pp. 2585-2593 ◽  
Author(s):  
Rafael L Rodríguez ◽  
Karthik Ramaswamy ◽  
Reginald B Cocroft

Mate choice is considered an important influence in the evolution of mating signals and other sexual traits, and—since divergence in sexual traits causes reproductive isolation—it can be an agent of population divergence. The importance of mate choice in signal evolution can be evaluated by comparing male signal traits with female preference functions, taking into account the shape and strength of preferences. Specifically, when preferences are closed (favouring intermediate values), there should be a correlation between the preferred values and the trait means, and stronger preferences should be associated with greater preference–signal correspondence and lower signal variability. When preferences are open (favouring extreme values), signal traits are not only expected to be more variable, but should also be shifted towards the preferred values. We tested the role of female preferences in signal evolution in the Enchenopa binotata species complex of treehoppers, a clade of plant-feeding insects hypothesized to have speciated in sympatry. We found the expected relationship between signals and preferences, implicating mate choice as an agent of signal evolution. Because differences in sexual communication systems lead to reproductive isolation, the factors that promote divergence in female preferences—and, consequently, in male signals—may have an important role in the process of speciation.

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Thomas G. Aubier ◽  
Hanna Kokko ◽  
Mathieu Joron

Abstract Sexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation. Theoretical studies have focused on the evolution of mate preferences in each sex separately. However, mounting empirical evidence suggests that premating isolation often involves mutual mate choice. Here, using a population genetic model, we investigate how female and male mate choice coevolve under a phenotype matching rule and how this affects reproductive isolation. We show that the evolution of female preferences increases the mating success of males with reciprocal preferences, favouring mutual mate choice. However, the evolution of male preferences weakens indirect selection on female preferences and, with weak genetic drift, the coevolution of female and male mate choice leads to periodic episodes of random mating with increased hybridization (deterministic ‘preference cycling’ triggered by stochasticity). Thus, counterintuitively, the process of establishing premating isolation proves rather fragile if both male and female mate choice contribute to assortative mating.


2018 ◽  
Author(s):  
Thomas G. Aubier ◽  
Hanna Kokko ◽  
Mathieu Joron

AbstractSexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation. Theoretical studies have focused on the evolution of mate preferences in each sex separately. However, mounting empirical evidence suggests that premating isolation often involves mutual mate choice. Here, using a population genetic model, we investigate how female and male mate choice coevolve under a phenotype matching rule and how this affects reproductive isolation. We show that the evolution of female preferences increases the mating success of males with reciprocal preferences, favouring mutual mate choice. However, the evolution of male preferences weakens indirect selection on female preferences and, with weak genetic drift, the coevolution of female and male mate choice leads to periodic episodes of random mating with increased hybridization (deterministic ‘preference cycling’ triggered by stochasticity). Thus, counterintuitively, the process of establishing premating isolation proves rather fragile if both male and female mate choice contribute to assortative mating.


2020 ◽  
Author(s):  
Yusan Yang ◽  
Corinne L Richards-Zawacki

Abstract Codivergence of sexual traits and mate preferences can lead to assortative mating and subsequently reproductive isolation. However, mate choice rarely operates without intrasexual competition, and the effects of the latter on speciation are often overlooked. Maintaining trait polymorphisms despite gene flow and limiting assortative female preferences for less-competitive male phenotypes are two important roles that male–male competition may play in the speciation process. Both roles rely on the assumption that male–male competition limits the expression of divergent female preferences. We tested this assumption in the highly color-polymorphic strawberry poison frog (Oophaga pumilio). Females prefer males of the local color, suggesting that reproductive isolation may be evolving among color morphs. However, this inference does not account for male–male competition, which is also color-mediated. We housed females with two differently colored males, and compared reproductive patterns when the more attractive male was the territory holder versus when he was the nonterritorial male. Females mated primarily with the territory winner, regardless of coloration, suggesting that when a choice must be made between the two, male territoriality overrides female preferences for male coloration. Our results highlight the importance of considering the combined effects of mate choice and intrasexual competition in shaping phenotypic divergence and speciation.


2020 ◽  
Vol 375 (1806) ◽  
pp. 20190546 ◽  
Author(s):  
Robin M. Tinghitella ◽  
Alycia C. R. Lackey ◽  
Catherine Durso ◽  
Jennifer A. H. Koop ◽  
Janette W. Boughman

Preference divergence is thought to contribute to reproductive isolation. Ecology can alter the way selection acts on female preferences, making them most likely to diverge when ecological conditions vary among populations. We present a novel mechanism for ecologically dependent sexual selection, termed ‘the ecological stage’ to highlight its ecological dependence. Our hypothesized mechanism emphasizes that males and females interact over mating in a specific ecological context, and different ecological conditions change the costs and benefits of mating interactions, selecting for different preferences in distinct environments and different male traits, especially when traits are condition dependent. We test key predictions of this mechanism in a sympatric three-spine stickleback species pair. We used a maternal half-sib split-clutch design for both species, mating females to attractive and unattractive males and raising progeny on alternate diets that mimic the specialized diets of the species in nature. We estimated the benefits of mate choice for an indicator trait (male nuptial colour) by measuring many fitness components across the lifetimes of both sons and daughters from these crosses. We analysed fitness data using a combination of aster and mixed models. We found that many benefits of mating with high-colour males depended on both species and diet. These results support the ecological stage hypothesis for sticklebacks. Finally, we discuss the potential role of this mechanism for other taxa and highlight its ability to enhance reproductive isolation as speciation proceeds, thus facilitating the evolution of strong reproductive isolation. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.


Author(s):  
Adélaïde Sibeaux ◽  
Thomas Camduras ◽  
John A Endler

Abstract The presence of various combinations of adjacent colors within polymorphic species’ color pattern could have a major impact on mate choice. We studied the role of pattern geometry in predicting mate choice in guppies using boundary strength analysis (BSA). BSA estimates the visual contrast intensity between two adjacent color patches (ΔS) weighted by the lengths of the boundaries between these adjacent color patches. We measured both the chromatic (hue and saturation) and achromatic (luminance) ΔS for each pair of adjacent patches. For each male’s color pattern, we measured BSA as both mean (mΔS) and coefficient of variation (cvΔS) of all ΔS weighted by their corresponding boundary lengths. We also determined if specific color patch boundaries had an impact on female preferences and whether these predicted overall male contrast (mΔS). We found that males with a higher mΔS were more attractive to females and that six boundaries containing either fuzzy black or black as one of the pair colors significantly affected female preferences, indicating that 1) females favored highly conspicuous males and 2) melanin-based patches could be used as a signal amplifier, not only for orange but for other colors.


2015 ◽  
Vol 282 (1816) ◽  
pp. 20151574 ◽  
Author(s):  
Matthew R. Wilkins ◽  
Daizaburo Shizuka ◽  
Maxwell B. Joseph ◽  
Joanna K. Hubbard ◽  
Rebecca J. Safran

Complex signals, involving multiple components within and across modalities, are common in animal communication. However, decomposing complex signals into traits and their interactions remains a fundamental challenge for studies of phenotype evolution. We apply a novel phenotype network approach for studying complex signal evolution in the North American barn swallow ( Hirundo rustica erythrogaster ). We integrate model testing with correlation-based phenotype networks to infer the contributions of female mate choice and male–male competition to the evolution of barn swallow communication. Overall, the best predictors of mate choice were distinct from those for competition, while moderate functional overlap suggests males and females use some of the same traits to assess potential mates and rivals. We interpret model results in the context of a network of traits, and suggest this approach allows researchers a more nuanced view of trait clustering patterns that informs new hypotheses about the evolution of communication systems.


2017 ◽  
Vol 284 (1852) ◽  
pp. 20170163 ◽  
Author(s):  
Sean T. Giery ◽  
Craig A. Layman

Natural selection plays an important role in the evolution of sexual communication systems. Here, we assess the effect of two well-known selection agents, transmission environment and predation, on interpopulation variation in sexual signals. Our model system is a series of 21 populations of Bahamian mosquitofish subjected to independent variation in optical conditions and predation risk. We show that optically diverse environments, caused by locally variable dissolved organic carbon concentrations, rather than spatial variation in predation, drove divergence in fin coloration (fin redness). We found a unimodal pattern of phenotypic variation along the optical gradient indicating a threshold-type response of visual signals to broad variation in optical conditions. We discuss evolutionary and ecological mechanisms that may drive such a pattern as well as the implications of non-monotonic clines for evolutionary differentiation.


2020 ◽  
Vol 375 (1806) ◽  
pp. 20190540 ◽  
Author(s):  
Henry L. North ◽  
Pierre Caminade ◽  
Dany Severac ◽  
Khalid Belkhir ◽  
Carole M. Smadja

Reinforcement has the potential to generate strong reproductive isolation through the evolution of barrier traits as a response to selection against maladaptive hybridization, but the genetic changes associated with this process remain largely unexplored. Building upon the increasing evidence for a role of structural variants in adaptation and speciation, we addressed the role of copy-number variation in the reinforcement of sexual isolation evidenced between the two European subspecies of the house mouse. We characterized copy-number divergence between populations of Mus musculus musculus that display assortative mate choice, and those that do not, using whole-genome resequencing data. Updating methods to detect deletions and tandem duplications (collectively: copy-number variants, CNVs) in Pool-Seq data, we developed an analytical pipeline dedicated to identifying genomic regions showing the expected pattern of copy-number displacement under a reinforcement scenario. This strategy allowed us to detect 1824 deletions and seven tandem duplications that showed extreme differences in frequency between behavioural classes across replicate comparisons. A subset of 480 deletions and four tandem duplications were specifically associated with the derived trait of assortative mate choice. These ‘Choosiness-associated’ CNVs occur in hundreds of genes. Consistent with our hypothesis, such genes included olfactory receptors potentially involved in the olfactory-based assortative mate choice in this system as well as one gene, Sp110 , that is known to show patterns of differential expression between behavioural classes in an organ used in mate choice—the vomeronasal organ. These results demonstrate that fine-scale structural changes are common and highly variable within species, despite being under-studied, and may be important targets of reinforcing selection in this system and others. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.


2019 ◽  
Vol 374 (1768) ◽  
pp. 20180183 ◽  
Author(s):  
Lukas Fuxjäger ◽  
Sylvia Wanzenböck ◽  
Eva Ringler ◽  
K. Mathias Wegner ◽  
Harald Ahnelt ◽  
...  

Plasticity, both within and across generations, can shape sexual traits involved in mate choice and reproductive success, and thus direct measures of fitness. Especially, transgenerational plasticity (TGP), where parental environment influences offspring plasticity in future environments, could compensate for otherwise negative effects of environmental change on offspring sexual traits. We conducted a mate choice experiment using stickleback ( Gasterosteus aculeatus ) with different thermal histories (ambient 17°C or elevated 21°C) within and across generations under simulated ocean warming using outdoor mesocosms. Parentage analysis of egg clutches revealed that maternal developmental temperature and reproductive (mesocosm) environment affected egg size, with females that developed at 17°C laying smaller eggs in 21°C mesocosms, likely owing to metabolic costs at elevated temperature. Paternal developmental temperature interacted with the reproductive environment to influence mating success, particularly under simulated ocean warming, with males that developed at 21°C showing lower overall mating success compared with 17°C males, but higher mating success in 21°C mesocosms. Furthermore, mating success of males was influenced by the interaction between F1 developmental temperature and F0 parent acclimation temperature, demonstrating the potential role of both TGP and within-generation plasticity in shaping traits involved in sexual selection and mate choice, potentially facilitating rapid responses to environmental change. This article is part of the theme issue ‘The role of plasticity in phenotypic adaptation to rapid environmental change’.


2002 ◽  
Vol 357 (1420) ◽  
pp. 471-492 ◽  
Author(s):  
Michele Drès ◽  
James Mallet

The existence of a continuous array of sympatric biotypes—from polymorphisms, through ecological or host races with increasing reproductive isolation, to good species—can provide strong evidence for a continuous route to sympatric speciation via natural selection. Host races in plant–feeding insects, in particular, have often been used as evidence for the probability of sympatric speciation. Here, we provide verifiable criteria to distinguish host races from other biotypes: in brief, host races are genetically differentiated, sympatric populations of parasites that use different hosts and between which there is appreciable gene flow. We recognize host races as kinds of species that regularly exchange genes with other species at a rate of more than ca . 1% per generation, rather than as fundamentally distinct taxa. Host races provide a convenient, although admittedly somewhat arbitrary intermediate stage along the speciation continuum. They are a heuristic device to aid in evaluating the probability of speciation by natural selection, particularly in sympatry. Speciation is thereby envisaged as having two phases: (i) the evolution of host races from within polymorphic, panmictic populations; and (ii) further reduction of gene flow between host races until the diverging populations can become generally accepted as species. We apply this criterion to 21 putative host race systems. Of these, only three are unambiguously classified as host races, but a further eight are strong candidates that merely lack accurate information on rates of hybridization or gene flow. Thus, over one–half of the cases that we review are probably or certainly host races, under our definition. Our review of the data favours the idea of sympatric speciation via host shift for three major reasons: (i) the evolution of assortative mating as a pleiotropic by–product of adaptation to a new host seems likely, even in cases where mating occurs away from the host; (ii) stable genetic differences in half of the cases attest to the power of natural selection to maintain multilocus polymorphisms with substantial linkage disequilibrium, in spite of probable gene flow; and (iii) this linkage disequilibrium should permit additional host adaptation, leading to further reproductive isolation via pleiotropy, and also provides conditions suitable for adaptive evolution of mate choice (reinforcement) to cause still further reductions in gene flow. Current data are too sparse to rule out a cryptic discontinuity in the apparently stable sympatric route from host–associated polymorphism to host–associated species, but such a hiatus seems unlikely on present evidence. Finally, we discuss applications of an understanding of host races in conservation and in managing adaptation by pests to control strategies, including those involving biological control or transgenic parasite–resistant plants.


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