Body Size and the Maintenance of Reproductive Isolation in Stickleback,Genus Gasterosteus

The blackspotted stickleback Gasterosteus wheatlandi and the widely studied threespine stickleback G. aculeatus are sympatric throughout the former’s range and share many aspects of life history and reproductive behaviour. These two species differ significantly in size, with G. wheatlandi of both sexes measured at approximately 60% of the standard length of their G. aculeatus counterparts. This study concentrated on G. wheatlandi courtship behaviour and investigated its role in the maintenance of reproductive isolation with G. aculeatus. Specifically, the roles that (1) female body size plays in influencing male courtship preferences and (2) male body size and behaviour play in female courtship preferences were investigated through dummy and live conspecific and heterospecific stimulus presentations. Male G. wheatlandi courtship preferences are consistent with previously described patterns for G. aculeatus. Males of both species preferentially approach and court the larger of two simultaneously presented live or dummy females. Thus, the smaller G. wheatlandi males are indiscriminate with respect to assortative mate choice; not only preferring to approach and court more fecund conspecific females but, more significantly, G. aculeatus‐sized females. In contrast, females of both species demonstrate strong assortative courtship preferences. When presented with pairs of flask‐enclosed males, females of both species preferentially orient and court the conspecific male over the heterospecific. Similarly, when presented with a conspecific male and a heterospecific male presented singly, females prefer to enter the nest of the conspecific. Systematic analysis of the interactions between these pairs of fish (one male, one female) demonstrates that the breakdown of courtship in heterospecific courtship occurs late in the courtship sequence when the widely differing forms of male leading behaviour results in drastically differing female responses. I suggest that, as previously described in G. aculeatus, the supernormality effect plays a significant role in mediating adaptive mate choice behaviour in G. wheatlandi. However, the added element of a larger sympatric species introduces a possible cost in time and energy devoted to courting heterospecific, and sympatric, females that the larger G. aculeatus do not likely incur. There is substantial evidence from many sympatric G. aculeatus species pairs that there is assortative mate choice based on size and/or courtship behaviour. Courtship trials suggest a more pervasive role for females in assortative mate choice. Whether it is male body size per se, or in combination with behaviour, morphology or other cues, is unresolved in the present study.     

Female mating preference functions predict sexual selection against hybrids between sibling species of cichlid fish

The evolutionary outcome of interspecific hybridization, i.e. collapse of species into a hybrid swarm, persistence or even divergence with reinforcement, depends on the balance between gene flow and selection against hybrids. If female mating preferences are open-ended but sign-inversed between species, they can theoretically be a source of such selection. Cichlid fish in African lakes have sustained high rates of speciation despite evidence for widespread hybridization, and sexual selection by female choice has been proposed as important in the origin and maintenance of species boundaries. However, it had never been tested whether hybridizing species have open-ended preference rules. Here we report the first experimental test using Pundamilia pundamilia, Pundamilia nyererei and their hybrids in three-way choice experiments. Hybrid males are phenotypically intermediate. Wild-caught females of both species have strong preferences for conspecific over heterospecific males. Their responses to F1 hybrid males are intermediate, but more similar to responses to conspecifics in one species and more similar to responses to heterospecifics in the other. We suggest that their mate choice mechanism may predispose haplochromine cichlids to maintain and perhaps undergo phenotypic diversification despite hybridization, and that species differences in female preference functions may predict the potential for adaptive trait transfer between hybridizing species.     

Linking intra‐ and interspecific assortative mating: Consequences for asymmetric sexual isolation

Assortative mating is of interest because of its role in speciation and the maintenance of species boundaries. However, we know little about how within‐species assortment is related to interspecific sexual isolation. Most previous studies of assortative mating have focused on a single trait in males and females, rather than utilizing multivariate trait information. Here, we investigate how intraspecific assortative mating relates to sexual isolation in two sympatric and congeneric damselfly species (genus Calopteryx). We connect intraspecific assortment to interspecific sexual isolation by combining field observations, mate preference experiments, and enforced copulation experiments. Using canonical correlation analysis, we demonstrate multivariate intraspecific assortment for body size and body shape. Males of the smaller species mate more frequently with heterospecific females than males of the larger species, which showed less attraction to small heterospecific females. Field experiments suggest that sexual isolation asymmetry is caused by male preferences for large heterospecific females, rather than by mechanical isolation due to interspecific size differences or female preferences for large males. Male preferences for large females and male–male competition for high quality females can therefore counteract sexual isolation. This sexual isolation asymmetry indicates that sexual selection currently opposes a species boundary.     

Female disdain for swords in a swordtail fish

Studies of mate choice evolution tend to focus on how female mating preferences are acquired and how they select for greater elaboration of male traits. By contrast, far less is known about how female preferences might be lost or reversed. In swordtail fish Xiphophorus, female preference for the sword ornament is an ancestral trait. Xiphophorus birchmanni, however, is one species that has secondarily lost the sword. Using synthetic animation playback of "virtual" males, we found that female X. birchmanni preferred a swordless conspecific over a sworded heterospecific. Moreover, when offered the choice between a conspecific without a sword and one with a digitally attached sword, females preferred the former. These results suggest female preferences need not always select for elaboration of male traits, and they provide a plausible explanation for the lack of introgression of a sexual trait in a naturally occurring hybrid zone.     

The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation

Females of many species are frequently courted by promiscuous males of their own and other closely related species. Such mating interactions may impose strong selection on female mating preferences to favor trait values in conspecific males that allow females to discriminate them from their heterospecific rivals. We explore the consequences of such selection in models of the evolution of female mating preferences when females must interact with heterospecific males from which they are completely postreproductively isolated. Specifically, we allow the values of both the most preferred male trait and the tolerance of females for males that deviate from this most preferred trait to evolve. Also, we consider situations in which females base their mating decisions on multiple male traits and must interact with males of multiple species. Females will rapidly differentiate in preference when they sometimes mistake heterospecific males for suitable mates, and the differentiation of female preference will select for conspecific male traits to differentiate as well. In most circumstances, this differentiation continues indefinitely, but slows substantially once females are differentiated enough to make mistakes rare. Populations of females with broader preference functions (i.e., broader tolerance for males with trait values that deviate from females' most preferred values) will evolve further to differentiate if the shape of the function cannot evolve. Also, the magnitude of separation that evolves is larger and achieved faster when conspecific males have lower relative abundance. The direction of differentiation is also very sensitive to initial conditions if females base their mate choices on multiple male traits. We discuss how these selection pressures on female mate choice may lead to speciation by generating differentiation among populations of a progenitor species that experiences different assemblages of heterospecifics. Opportunities for differentiation increase as the number of traits involved in mate choice increase and as the number of species involved increases. We suggest that this mode of speciation may have been particularly prevalent in response to the cycles of climatic change throughout the Quaternary that forced the assembly and disassembly of entire communities on a continentwide basis.     

REPRODUCTIVE BEHAVIOR OF FEMALE BUNTINGS: ISOLATING MECHANISMS IN A HYBRIDIZING PAIR OF SPECIES

The plumage characteristics of male Indigo and Lazuli Buntings are distinct, but the two species can learn each other's songs. Populations comprising Indigo, Lazuli and hybrid individuals occur in the Great Plains of North America, and assortative mating has been inferred from morphometric data. We devised a laboratory assay for determining female preferences for visual and vocal characteristics of conspecific and heterospecific males and for mixtures of these characteristics, such as might be encountered in an overlap population. Females of both species gave more copulation-solicitation displays when exposed to conspecific plumage and vocalizations than when exposed to heterospecific plumage and vocalizations. Females gave intermediate and similar responses to the combinations of conspecific plumage with heterospecific vocalizations and heterospecific plumage with conspecific vocalizations. Thus, in the absence of other potentially important variables, female reproductive behavior is consistent with the hypothesis of assortative mating, based upon both vocal and visual traits of the males and caused by female choice in this semispecies pair.     

The Strength of Species Recognition in Captive Female Zebra Finches (Taeniopygia guttata): A Comparison Across Estrildid Heterospecifics

Conspecific recognition is essential for sexually reproducing species. Captive zebra finches ( Taeniopygia guttata ) are a model system in which the behavioural, ontogenetic and neurobiological bases of own-species (conspecific) recognition have been studied in detail. To assess the potential role of phylogeographic effects on species recognition, we examined the spatial preferences of unmated captive-bred female zebra finches between unfamiliar captive males of conspecific and estrildid heterospecific male stimuli. In accordance with prior studies using domesticated Bengalese finches ( Lonchura striata vars. domestica ), we found significant spatial and behavioural preference for conspecific males by female zebra finches, irrespective of heterospecific male phylogeographic origin mating status, or individual behaviour. This result has ramifications for the interpretation of social and mate preferences in this model species as it implies a consistency of species discrimination by captive female zebra finches.     

Differential responses of yellow-breasted chats, Icteria virens, to male and female conspecific model presentations

A detailed understanding of the behavioural interactions between males and females is crucial for elucidating the selection pressures shaping mating system evolution; however, these interactions are often difficult to observe, particularly in free-living populations. We simulated extraterritorial intrusions by presenting conspecific models on to territories of a Neotropical migratory passerine, the yellow-breasted chat, Icteria virens. Simulated intrusions elicited different responses based on the sex of the focal individual and the sex and species of the model. Behavioural responses of the focal individuals were largely directed towards conspecific models, whereas simulated heterospecific intrusions, using a Carolina wren, Thryothorus ludovicianus, model, elicited minimal response. Male song was not related to any particular model presentation. Males directed mating behaviours, including courtship displays and copulations, exclusively towards the female conspecific model. Males behaved aggressively towards the conspecific male model. In contrast, females never showed any courtship behaviour towards the male model and showed significant aggression towards the conspecific female model. The results of this study reveal that territorial aggression in yellow-breasted chats is strongly intrasexual. Additionally, simulated female extraterritorial intrusions, but not male intrusions, resulted in extrapair courtship and copulation. This pattern is likely to be typical of many socially monogamous species and points to the behavioural mechanisms underlying both monogamy and extrapair mating systems.     

Turbidity affects association behaviour in male Poecilia latipinna

Male association preferences in a bisexual‐unisexual species complex were studied in clear and turbid environments. In south and central Texas, where the gynogenetic sexual‐parasite Poecilia formosa lives syntopically with Poecilia latipinna as its sexual host species, association times of P. latipinna males with conspecific sexual and heterospecific asexual females in clear and turbid water were measured sequentially. Turbidity had an influence on male mate association behaviour. Males spent less time with any kind of female stimulus in turbid water. There was no preference for conspecific sexual females, either in turbid water or under clear conditions. Also, origin of males and acclimatization to turbid water had no effect. How turbidity as a source of visual noise might affect communication among individuals and how this environmental factor might contribute to the stability of this sexual‐asexual mating complex in nature are discussed.     

REINFORCEMENT OF STICKLEBACK MATE PREFERENCES: SYMPATRY BREEDS CONTEMPT

Detailed studies of reproductive isolation and how it varies among populations can provide valuable insight into the mechanisms of speciation. Here we investigate how the strength of premating isolation varies between sympatric and allopatric populations of threespine sticklebacks to test a prediction of the hypothesis of reinforcement: that interspecific mate discrimination should be stronger in sympatry than in allopatry. In conducting such tests, it is important to control for ecological character displacement between sympatric species because ecological character divergence may strengthen prezygotic isolation as a by-product. We control for ecological character displacement by comparing mate preferences of females from a sympatric population (benthics) with mate preferences of females from two allopatric populations that most closely resemble the sympatric benthic females in ecology and morphology. No-choice mating trials indicate that sympatric benthic females mate less readily with heterospecific (limnetic) than conspecific (benthic) males, whereas two different populations of allopatric females resembling benthics show no such discrimination. These differences demonstrate reproductive character displacement of benthic female mate choice. Previous studies have established that hybridization between sympatric species occurred in the past in the wild and that hybrid offspring have lower fitness than either parental species, thus providing conditions under which natural selection would favor individuals that do not hybridize. Results are therefore consistent with the hypothesis that female mate preferences have evolved as a response to reduced hybrid fitness (reinforcement), although direct effects of sympatry or a biased extinction process could also produce the pattern. Males of the other sympatric species (limnetics) showed a preference for smaller females, in contrast to the inferred ancestral preference for larger females, suggesting reproductive character displacement of limnetic male mate preferences as well.     

Identifying female phenotypes that promote behavioral isolation in a sexually dimorphic species of fish Etheostoma zonale

In sexually dimorphic species characterized by exaggerated male ornamentation, behavioral isolation is often attributed to female preferences for conspecific male signals. Yet, in a number of sexually dimorphic species, male mate choice also results in behavioral isolation. In many of these cases, the female traits that mediate species boundaries are unclear. Females in sexually dimorphic species typically lack many of the elaborate traits that are present in males and that are often used for taxonomic classification of species. In a diverse and largely sexually dimorphic group of fishes called darters (Percidae: Etheostoma), male mate choice contributes to behavioral isolation between a number of species; however, studies addressing which female traits males prefer are lacking. In this study, we identified the dominant female pattern for two sympatric species, Etheostoma zonale and Etheostoma barrenense, using pattern energy analysis, and we used discriminate function analysis to identify which aspects of female patterning can reliably classify species. We then tested the role of female features in male mate choice for E. zonale, by measuring male preference for computer animations displaying the identified (species-specific) conspecific features. We found that the region above the lateral line is important in mediating male mate preferences, with males spending a significantly greater proportion of time with animations exhibiting conspecific female patterning in this region than with animations exhibiting heterospecific female patterning. Our results suggest that the aspects of female phenotypes that are the target of male mate choice are different from the conspicuous male phenotypes that traditionally characterize species.     

Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish

Theory suggests that genetic polymorphisms in female mating preferences may cause disruptive selection on male traits, facilitating phenotypic differentiation despite gene flow, as in reinforcement or other models of speciation with gene flow. Very little experimental data have been published to test the assumptions regarding the genetics of mate choice that such theory relies on. We generated a population segregating for female mating preferences and male colour dissociated from other species differences by breeding hybrids between species of the cichlid fish genus Pundamilia. We measured male mating success as a function of male colour. First, we demonstrate that non-hybrid females of both species use male nuptial coloration for choosing mates, but with inversed preferences. Second, we show that variation in female mating preferences in an F2 hybrid population generates a quadratic fitness function for male coloration suggestive of disruptive selection: intermediate males obtained fewer matings than males at either extreme of the colour range. If the genetics of female mate choice in Pundamilia are representative for those in other species of Lake Victoria cichlid fish, it may help explain the origin and maintenance of phenotypic diversity despite some gene flow.     

Sex-specific territorial responses in Tawny Owls Strix aluco

A territorial intruder often poses more of a threat to the territory holder of the same sex as itself. As territorial aggression is associated with costs, aggression shown by birds towards territorial intruders of the opposite sex deserves investigation. This behaviour could arise due to the reproductive value of a mate or through mutualism between members of a pair. We investigated these hypotheses by presenting mated pairs of Tawny Owls Strix aluco with playback of male calls, female calls and a male and female duetting, and recording the number and intensity of responses by the male and female territory holders. Females responded significantly more often to female than to male calls. Males responded equally often to male and female playback. Males which had previously bred successfully with their mate were significantly more likely to respond to female playback in the spring, which suggested males were responding to female playback due to the reproductive value of their mate. There was no evidence of mutualism between members of a pair.     

Character displacement and the evolution of mate choice: an artificial neural network approach

Interactions with heterospecifics can promote the evolution of divergent mating behaviours between populations that do and do not occur with heterospecifics. This process--reproductive character displacement--potentially results from selection to minimize the risk of mating with heterospecifics. We sought to determine whether heterospecific interactions lead to divergence of female preferences for aspects of conspecific male signals. We used artificial neural network models to simulate a mate recognition system in which females co-occur with different heterospecifics in different populations. Populations that evolved conspecific recognition in the presence of different heterospecifics varied in their preferences for aspects of conspecific male signals. When we tested networks for their preferences of conspecific versus heterospecific signals, however, we found that networks from allopatric populations were usually able to select against heterospecifics. We suggest that female preferences for aspects of conspecific male signals can result in a concomitant reduction in the likelihood that females will mate with heterospecifics. Consequently, even females in allopatry may discriminate against heterospecific mates depending on the nature of their preferences for conspecifics. Such a pattern could potentially explain cases where reproductive character displacement is expected, but not observed.     

Incomplete behavioural isolation and asymmetric female preference in darter sister species (Percidae: Etheostoma)

In this study, female preferences and behavioural isolation were estimated in a pair of allopatric sister species, Etheostoma duryi and Etheostoma flavum. Dichotomous mate preference trials were conducted to determine whether females prefer to associate with conspecific over heterospecific males and free‐spawning assays were conducted to determine whether those preferences translated into behavioural isolation. Dichotomous mate choice trials revealed asymmetric female preference, as female E. flavum preferred conspecific males, whereas female E. duryi showed no preference. Free‐spawning assays indicated that behavioural isolation remains incomplete between E. duryi and E. flavum (I_B = 0·19). In addition to female mating preferences, male behaviour also appeared to influence mating outcomes as male E. flavum consistently courted conspecific females more often in free‐spawning assays whereas male E. duryi did not. The data therefore suggest that despite marked divergence in male nuptial colour, divergence in female preferences between these species may not be sufficient to maintain species boundaries upon secondary contact. These results contrast with similar work in a sympatric darter species pair and may be explained by considering the contributions of reinforcement and differences in colour pattern as well as colour value.     

Assortative aggression among males in a sympatric pair of Labeotropheus from Lake Malaŵi,Africa

Female mate choice has strong experimental support as a diversifying force in the speciation of the haplochromine cichlid fishes of Lake Malaŵi, Africa. Somewhat less understood is the role that male–male aggression might have played in the evolution of new species of these fishes. In the rock-dwelling haplochromines of Lake Malaŵi, primarily territory-holding males successfully court females; by determining which males gain territories, male–male aggression could support speciation by excluding less-fit males from the breeding population. To test the hypothesis that males should direct more aggression towards conspecific rivals, the aggression directed towards conspecific and heterospecific opponents was compared in a sympatric pair of cichlids of the genus Labeotropheus Ahl 1927 (Labeotropheus fuelleborni Ahl 1927 and Labeotropheus trewavasae Fryer 1956). It was found that when presented with a pair of rivals, males of both species did direct more aggression towards the conspecific opponent, and the amount of aggression increased when the conspecific opponent was larger than the heterospecific opponent. In addition, this study found a difference in the behavioural repertoire of the species: L. fuelleborni tends to rely on displays to intimidate opponents, whereas L. trewavasae employs more physical attacks to drive away opponents. Males of both species can thus recognize conspecifics and assess an opponent's relative threat to their ability to successfully reproduce, and use species-specific strategies to intimidate opponents.     

Species recognition by male swordtails via chemical cues

Species recognition can often play a key role in female matingpreferences. Far less is known about conspecific mate recognitionfrom the male perspective. In many closely related taxa, femalesexhibit few obvious visual differences and males might haveto attend to chemical cues in mate recognition, a possibilitythat has rarely been explored in vertebrates. Here, we examinemale species recognition via odor cues in the swordtail fish,Xiphophorus birchmanni. In dichotomous choice experiments wefirst tested whether males respond to female odor cues. We foundthat males were attracted to conspecific female odor and thoseof a related allopatric congener, Xiphophorus malinche, overa water control. Males did not, however, respond to the femaleodor of the more distantly related sympatric platyfish, Xiphophorusvariatus. We then gave male X. birchmanni the choice betweenconspecific and heterospecific female stimuli. Males, in thisscenario, significantly preferred the conspecific odor whenthe alternative was platyfish. However, when offered odor cuesof X. malinche, male X. birchmanni actually preferred the heterospecificfemale cue. The complex array of preferences reported here,previously documented only in females, underscores the needto consider the behavior of both sexes in dictating actual matingoutcomes.     

Males,but not females,contribute to sexual isolation between two sympatric species of <Emphasis Type="Italic">Gambusia</Emphasis>

Reproductive isolation restricts genetic exchange between species. Various pre- and post-mating barriers, such as behavior, physiology and gametic incompatibility, have been shown to evolve in sympatry. In certain scenarios, isolation can be asymmetrical, where species differentially prefer conspecifics. We examined sexual isolation via conspecific mate preference between Gambusia affinis and G. geiseri in both sexes. To investigate male contribution to sexual isolation, we compared the number of mating attempts (gonopodial thrusts) directed at either a conspecific or a heterospecific female, in both species. We also examined sperm priming and expenditure in males in the presence of conspecific or heterospecific females. We then measured female preference for either a conspecific or heterospecific male, in both species. We found that males of both species preferred to mate with conspecific females, but showed no difference in sperm production or expenditure between conspecific and heterospecific females. Females of both species did not prefer conspecific over heterospecific males. Our results suggest that sexual isolation might be mediated by male mate choice in this system and not female choice, suggesting that there is asymmetrical reproductive isolation between the sexes in G. affinis and G. geiseri, but symmetrical species isolation.     

Aggressive biases towards similarly coloured males in Lake Malawi cichlid fishes

In haplochromine cichlids, female mate choice based on male nuptial coloration has played an important role in speciation. Recent studies suggest that male coloration strongly influences the distribution of these fishes based on male-male aggression; males direct more aggression towards similarly coloured opponents while tolerating differently coloured individuals. We explored the role of male nuptial colour in aggression among the mbuna of Lake Malawi, examining aggression by male Metriaclima mbenjii, the red top cobalt zebra, towards conspecific opponents, similarly coloured heterospecific opponents and differently coloured heterospecifics. In trials in which focal males were offered a single opponent, while the total number of aggressive behaviours did not vary among opponent species, the types of behaviours did; focal males directed more lateral displays towards conspecifics than towards the other opponent species. When focal males were offered two opponents simultaneously, M. mbenjii directed more aggressive behaviours and more lateral displays towards similarly coloured opponents, regardless of species. Furthermore, when offered a conspecific and a similarly coloured opponent simultaneously, there were no differences in behaviour towards either opponent. Thus, nuptial coloration is used by males to identify competitors, and it suggests that male-male aggression may have also been an important diversifying force in speciation in rock-dwelling Lake Malawi cichlids.     

Male-male competition and speciation: aggression bias towards differently coloured rivals varies between stages of speciation in a Lake Victoria cichlid species complex

Sympatric speciation driven by sexual selection by female mate choice on a male trait is a much debated topic. The process is problematic because of the lack of negative frequency-dependent selection that can facilitate the invasion of a novel colour phenotype and stabilize trait polymorphism. It has recently been proposed that male-male competition for mating territories can generate frequency-dependent selection on male colouration. Rare male cichlid fish would enjoy a fitness advantage if territorial defenders bias aggression towards male cichlid fish of their own colour. We used blue (ancestral type) and red phenotypes of the Lake Victoria cichlid species complex Pundamilia. We tested the aggression bias of wild-caught territorial blue male cichlid fish from five separate populations for blue vs. red rival male cichlid fish using simulated intruder choice tests. The different populations vary in the frequency of red male cichlid fish, and in the degree of reproductive isolation between red and blue, reflecting different stages of speciation. Blue male cichlid fish from a population that lack red phenotypes biased aggression towards blue stimulus male cichlid fish. The same was found in two populations where blue and red are reproductively isolated sister species. This aggression bias may facilitate the invasion of a novel colour phenotype and species coexistence. Blue male cichlid fish from two populations where red and blue are hybridizing incipient species biased aggression towards red stimulus male cichlid fish. Thus, after a successful invasion of red, aggression bias alone is not likely to generate frequency dependence required to stabilize the coexistence of phenotypes. The findings show that aggression bias varies between stages of speciation, but is not enough to stabilize the process of speciation.