Sexual selection promotes hybridization between Pecos pupfish, Cyprinodon pecosensis and sheepshead minnow, C. variegatus

Rapid and extensive genetic introgression has occurred between Pecos pupfish (Cyprinodon pecosensis) and sheepshead minnow (Cyprinodon variegatus) in the wild. We studied both female mate choice and male-male competition for mates among C. pecosensis, C. variegatus, and their F1 hybrids to determine what role these behaviours played in the formation of the hybrid swarm. Female C. pecosensis preferred male C. variegatus to conspecific males, C. variegatus females displayed no significant preference when given a choice between purebred males, and neither C. pecosensis nor C. variegatus females discriminated against F1 hybrid males. We found no evidence for female olfactory recognition of mates. Male F1 hybrids and C. variegatus were more aggressive than C. pecosensis males, achieving greater reproductive success under two different experimentally-induced mating systems. Hybrids were superior to C. variegatus when only two males competed (dominance interactions), but the two types were competitively equivalent in a territorial mating system. Our results indicate that active inter- and intra-sexual selection contributed to the accelerated hybridization between these two species. By including the possibility that some aspects of a hybridization and introgression event may be under positive selection, researchers may better understand the dynamics that lead to hybrid zone stability or the spread of introgressed genetic material.     

Nonadaptive female pursuit of extrapair copulations can evolve through hitchhiking

Mounting evidence has indicated that engaging in extrapair copulations (EPCs) might be maladaptive or detrimental to females. It is unclear why such nonadaptive female behavior evolves. In this study, we test two hypotheses about the evolution of female EPC behavior using population genetic models. First, we find that both male preference for allocating extra effort to seek EPCs and female pursuit behavior without costs can be maintained and remain polymorphic in a population via frequency‐dependent selection. However, both behaviors cannot evolve when females with pursuit behavior suffer from a decline in male parental care. Second, we present another novel way in which female pursuit behavior can evolve; indirect selection can act on this behavior through a ratchet‐like mechanism involving oscillating linkage disequilibria between the target EPC pursuit locus and two other loci determining male mate choice and a female sexual signal. Although the overall positive force of such indirect selection is relatively weak, our results suggest that it may still play a role in promoting the evolution of female EPC behavior when this behavior is nonadaptive (i.e., it is neutral) or only somewhat maladaptive (e.g., males only occasionally lower parental care when their mates pursue EPCs).     

Bucking the Trend in Wolf-Dog Hybridization: First Evidence from Europe of Hybridization between Female Dogs and Male Wolves

Studies on hybridization have proved critical for understanding key evolutionary processes such as speciation and adaptation. However, from the perspective of conservation, hybridization poses a concern, as it can threaten the integrity and fitness of many wild species, including canids. As a result of habitat fragmentation and extensive hunting pressure, gray wolf (Canis lupus) populations have declined dramatically in Europe and elsewhere during recent centuries. Small and fragmented populations have persisted, but often only in the presence of large numbers of dogs, which increase the potential for hybridization and introgression to deleteriously affect wolf populations. Here, we demonstrate hybridization between wolf and dog populations in Estonia and Latvia, and the role of both genders in the hybridization process, using combined analysis of maternal, paternal and biparental genetic markers. Eight animals exhibiting unusual external characteristics for wolves - six from Estonia and two from Latvia - proved to be wolf-dog hybrids. However, one of the hybridization events was extraordinary. Previous field observations and genetic studies have indicated that mating between wolves and dogs is sexually asymmetrical, occurring predominantly between female wolves and male dogs. While this was also the case among the Estonian hybrids, our data revealed the existence of dog mitochondrial genomes in the Latvian hybrids and, together with Y chromosome and autosomal microsatellite data, thus provided the first evidence from Europe of mating between male wolves and female dogs. We discuss patterns of sexual asymmetry in wolf-dog hybridization.     

Female Sexual Preferences Toward Conspecific and Hybrid Male Mating Calls in Two Species of Polygynous Deer, <Emphasis Type="Italic">Cervus elaphu</Emphasis>s and <Emphasis Type="Italic">C. nippon</Emphasis>

The behavioral processes at the basis of hybridization and introgression are understudied in terrestrial mammals. We use a unique model to test the role of sexual signals as a reproductive barrier to introgression by investigating behavioral responses to male sexual calls in estrous females of two naturally allopatric but reproductively compatible deer species, red deer and sika deer. Previous studies demonstrated asymmetries in acoustic species discrimination between these species: most but not all female red deer prefer conspecific over sika deer male calls while female sika deer exhibit no preference differences. Here, we extend this examination of acoustic species discrimination to the role of male sexual calls in introgression between parent species and hybrids. Using two-speaker playback experiments, we compared the preference responses of estrous female red and sika deer to male sexual calls from conspecifics versus red × sika hybrids. These playbacks simulate early secondary contact between previously allopatric species after hybridization has occurred. Based on previous conspecific versus heterospecific playbacks, we predicted that most female red deer would prefer conspecific calls while female sika deer would show no difference in their preference behaviors toward conspecific and hybrid calls. However, results show that previous asymmetries did not persist as neither species exhibited more preferences for conspecific over hybrid calls. Thus, vocal behavior is not likely to deter introgression between these species during the early stages of sympatry. On a wider scale, weak discrimination against hybrid sexual signals could substantially contribute to this important evolutionary process in mammals and other taxa.     

Can alternative mating tactics facilitate introgression across a hybrid zone by circumventing female choice?

Reproductive barriers and divergence in species’ mate recognition systems underlie major models of speciation. However, hybridization between divergent species is common, and classic mechanisms to explain permeable reproductive barriers rarely consider how an individual may attain reproductive success. Alternative mating tactics (AMTs) exist in various forms across animal taxa. Such tactics may allow poorer quality individuals to gain mating opportunities and facilitate introgression either through asymmetrical positive selection or by circumventing female choice altogether in areas of secondary contact. One such tactic is satellite behaviour in frogs, where silent males perch near advertisers in an attempt to intercept females. To test whether such satellite male tactics are context‐dependent and favoured by hybrids, we genotyped and quantified the morphology of 80 male spring peeper (Pseudacris crucifer) individuals involved in caller–satellite associations from a secondary contact zone between two intraspecific mitochondrial lineages. Irrespective of population, satellite behaviour was best predicted by size but not body condition. Within the contact zone, pure individuals showed a significantly greater probability of being active callers, whereas hybrids of one lineage were more likely to adopt the satellite tactic. We suggest that satellite behaviour in P. crucifer promotes introgression, breaks down reproductive isolating barriers and contributes to asymmetrical introgression in this secondary contact zone. AMTs may thus be an underexplored but important alternative to oft‐discussed causes of genetic discordance found in hybrid zones.     

PATTERNS OF SPECIATION IN DROSOPHILA

To investigate the time course of speciation, we gathered literature data on 119 pairs of closely related Drosophila species with known genetic distances, mating discrimination, strength of hybrid sterility and inviability, and geographic ranges. Because genetic distance is correlated with divergence time, these data provide a cross-section of taxa at different stages of speciation. Mating discrimination and the sterility or inviability of hybrids increase gradually with time. Hybrid sterility and inviability evolve at similar rates. Among allopatric species, mating discrimination and postzygotic isolation evolve at comparable rates, but among sympatric species strong mating discrimination appears well before severe sterility or inviability. This suggests that prezygotic reproductive isolation may be reinforced when allopatric taxa become sympatric. Analysis of the evolution of postzygotic isolation shows that recently diverged taxa usually produce sterile or inviable male but not female hybrids. Moreover, there is a large temporal gap between the evolution of male-limited and female hybrid sterility or inviability. This gap, which is predicted by recent theories about the genetics of speciation, explains the overwhelming preponderance of hybridizations yielding male-limited hybrid sterility or inviability (Haldane's rule).     

Evidence for strong assortative mating,limited gene flow,and strong differentiation across the blue‐footed/Peruvian booby hybrid zone in northern Peru

Hybrid zones represent natural laboratories in which the processes of divergence and genetic isolation can be examined. The generation and maintenance of a hybrid zone requires mispairing and successful reproduction between organisms that differ in one or more heritable traits. Understanding the dynamics of hybridization between two species requires an understanding of the extent to which they have diverged genetically, the frequency of misparing and hybrid production, and the extent of introgression. Three hundred and twenty one blue‐footed Sula nebouxii and Peruvian S. variegata boobies from the eastern tropical Pacific Ocean were analyzed using 19 putatively neutral genetic markers to evaluate interspecific differentiation, to classify morphological hybrids using Bayesian assignments, and to characterize hybridization using cline theory and Bayesian assignments. The species were well differentiated at mitochondrial and nuclear microsatellites, the hybrid zone was bimodal (contained a high frequency of each parental species but a low frequency of hybrids), and morphologically intermediate individuals were most likely F1 hybrids resulting from mating between female Peruvian boobies and male blue‐footed boobies. Clines in allele frequency could be constrained to share a common geographic centre but could not be constrained to share a common width. Peruvian and blue‐footed boobies hybridize infrequently, potentially due to strong premating reproductive isolation; however, backcrossing appears to facilitate introgression from blue‐footed to Peruvian boobies in this hybrid system.     

Speciation by Reinforcement: A Model Derived from Studies of Drosophila

Reinforcement is an increase in premating reproductive isolation between taxa resulting from selection against hybrids. We present a model of reinforcement with a novel type of selection on female mating behavior. Previous models of reinforcement have focused on the divergence of female mating preferences between nascent species. We suggest that an increase in the level of female mating discrimination can yield reinforcement without further divergence of either male characters or female preferences. This model indicates that selection on mating discrimination is a viable mechanism for reinforcement and may allow speciation under less stringent conditions than selection on female preference. This model also incorporates empirical results from genetic studies of hybrid fitness determination in Drosophila species. We find that the details of inheritance, which include sex-linked transmission, sex-limited fertility reduction, and X-autosome epistasis, have important effects on the likelihood of reinforcement. In particular, X-autosome epistasis for hybrid fitness determination facilitates reinforcement when hybrid fertility reduction occurs in males, but hinders the process when it occurs in females. HALDANE's rule indicates that hybrid sterility will generally evolve in males prior to females within nascent species. Thus, HALDANE's rule and X-autosome epistasis provide conditions that are surprisingly favorable for reinforcement in Drosophila.     

REPRODUCTIVE PATTERNS SHAPE INTROGRESSION DYNAMICS AND SPECIES SUCCESSION WITHIN THE EUROPEAN WHITE OAK SPECIES COMPLEX

The reproductive system of hybrids is an important factor shaping introgression dynamics within species complexes. We combined paternity and parentage analyses with previous species characterization by genetic assignment, to directly identify reproductive events that occurred within a stand comprising four European white oak species. Comparing species status of parent pairs provided a precise quantification of hybridization rate, backcrosses, and intraspecific matings in two life stages. The detailed mating system analysis revealed new findings on the dynamics of interspecific gene flow. First, hybrids acted successfully as both male and female during reproduction. They produced acorns and seedlings that were as viable as those sired by purebreds. Second, species maintenance could be due to a relatively low level of interspecific mating contrasting with a large proportion of intraspecific crosses and backcrosses. Despite a high proportion of hybrids and extensive interspecific gene flow, partial species integrity is maintained by genetically controlled pollen discrimination, ensuring preferential matings within purebreds and high parental species fidelity in hybrid reproduction, which impedes complete collapse into a continuous hybrid swarm. Finally, we showed that pollen from the different species had unequal contributions to reproduction suggesting that introgression processes could ultimately lead to extirpation or expansion of some species.     

The costs of choice in sexual selection

In Fisher's model of sexual selection female mating preferences are not subject to direct selection but evolve purely because they are genetically correlated with the favoured male trait. But when female choice is costly relative to random mating, for example in energy, time or predation risks, the evolution of female mating preference is subject also to direct selection. With costly female choice the set or line of equilibria found in models of Fisher's process no longer exists. On the line the male trait is under zero net selection, and there is no advantage for a female choosing a male with a more exaggerated character. Therefore any cost to choice causes choosiness to decline. In turn this lowers the strength of sexual selection and the male trait declines as well. So when Fisher's process is the sole force of sexual selection and female choice is costly, only transitory increases in female choice and the preferred male trait are possible. It has often been claimed that exaggerated male characters act as markers or revealers of the genetic quality of potential mates. If females choose their mates using traits that correlate with heritable viability differences then stable exaggeration of both female choice and the preferred male character is possible, even when female choice is costly. The offspring of choosy females have not only a Fisherian reproductive advantage but also greater viability. This suggests that in species with exaggerated male ornamentation, in which female choice is costly, it is likely that female mate choice will be for traits that correlate with male genetic quality.     

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.     

Introgressive hybridization as a mechanism for species rescue

Rapid evolution on ecological time scales can play a key role in species responses to environmental change. One dynamic that has the potential to generate the diversity necessary for evolution rapid enough to allow response to sudden environmental shifts is introgressive hybridization. However, if distinct sub-species exist before an environmental shift, mechanisms that impede hybridization, such as assortative mating and hybrid inferiority, are likely to be present. Here we explore the theoretical potential for introgressive hybridization to play a role in response to environmental change. In particular, we incorporate assortative mating, hybrid inferiority, and demographic stochasticity into a two-locus, two-allele population genetic model of two interacting species where one locus identifies the species and the other determines how fitness depends on the changing environment. Simulation results indicate that moderately high values for the strength of assortative mating will allow enough hybridization events to outweigh demographic stochasticity but not so many that continued hybridization outweighs backcrossing and introgression. Successful introgressive hybridization also requires intermediate relative fitness at the allele negatively affected by environmental change such that hybrid survivorship outweighs demographic stochasticity but selection remains strong enough to affect the genetic dynamics. The potential for successful introgression instead of extinction with greater environmental change is larger with monogamous rather than promiscuous mating due to lower stochasticity in mating events. These results suggest species characteristics (e.g., intermediate assortative mating and mating systems with low variation in mating likelihood) which indicate a potential for rapid evolution in response to environmental change via introgressive hybridization.     

Genetic characterization of hybridization and introgression between anadromous rainbow trout (Oncorhynchus mykiss irideus) and coastal cutthroat trout (O. clarki clarki)

Interspecific hybridization represents a dynamic evolutionary phenomenon and major conservation problem in salmonid fishes. In this study we used amplified fragment length polymorphisms (AFLP) and mitochondrial DNA (mtDNA) markers to describe the extent and characterize the pattern of hybridization and introgression between coastal rainbow trout (Oncorhynchus mykiss irideus) and coastal cutthroat trout (O. clarki clarki). Hybrid individuals were initially identified using principle coordinate analysis of 133 polymorphic AFLP markers. Subsequent analysis using 23 diagnostic AFLP markers revealed the presence of F1, rainbow trout backcross, cutthroat trout backcross and later-generation hybrids. mtDNA analysis demonstrated equal numbers of F1 hybrids with rainbow and cutthroat trout mtDNA indicating reciprocal mating of the parental types. In contrast, rainbow and cutthroat trout backcross hybrids always exhibited the mtDNA from the recurrent parent, indicating a male hybrid mating with a pure female. This study illustrates the usefulness of the AFLP technique for generating large numbers of species diagnostic markers. The pattern of hybridization raises many questions concerning the existence and action of reproductive isolating mechanisms between these two species. Our findings are consistent with the hypothesis that introgression between anadromous populations of coastal rainbow and coastal cutthroat trout is limited by an environment-dependent reduction in hybrid fitness.     

Hybridization and Introgression among Species of Sunfish (Lepomis): Analysis by Mitochondrial DNA and Allozyme Markers

We explore the potential of mitochondrial DNA (mtDNA) analysis, alone and in conjunction with allozymes, to study low-frequency hybridization and introgression phenomena in natural populations. MtDNAs from small samples of nine species of sunfish (Lepomis, Centrarchidae) were purified and digested with each of 13 informative restriction enzymes. Digestion profiles for all species were highly distinct: estimates of overall fragment homology between pairs of species ranged from 0-36%. Allozymes encoded by nine nuclear genes also showed large freqency differences among species and together with mtDNA provided many genetic markers for hybrid identification. A genetic analysis of 277 sunfish from two locations in north Georgia revealed the following: (1) a low frequency of interspecific hybrids, all of which appeared to be F1's; (2) the involvement of five sympatric Lepomis species in the production of these hybrids; (3) no evidence for introgression between species in our study locales (although for rare hybridization, most later-generation backcrosses would not be reliably distinguished from parentals); (4) a tendency for hybridizations to take place preferentially between parental species differing greatly in abundance; (5) a tendency for the rare species in a hybrid cross to provide the female parent. Our data suggest that absence of conspecific pairing partners and mating stimuli for females of rarer species may be important factors in increasing the likelihood of interspecific hybridization. The maternal inheritance of mtDNA offers at least two novel advantages for hybridization analysis: (1) an opportunity to determine direction in hybrid crosses; and (2) due to the linkage among mtDNA markers, an increased potential to distinguish effects of introgression from symplesiomorphy or character convergence.     

Reinforcement during ecological speciation.

Reinforcement of pre-zygotic isolation can result when any of several kinds of selection act against hybrids. This paper investigates the situation where hybrids are selected against for ecological reasons, for example when there is no niche for individuals that are phenotypically intermediate between the parental species. The calculations here show how much ecological selection can lead to the reinforcement of a female mating preference or an assortative mating trait that is expressed in both sexes. The model allows for the ecological trait to be affected by any number of loci, but assumes that selection is weak and the introgression rate small. The effect of selection against hybrids increases rapidly as the difference between the mean phenotypes of the two populations increases. When genetic variation in the ecological trait is caused by many loci, stabilizing selection on it further contributes to reinforcement.     

Rare and asymmetrical hybridization of the endemic Barbus carpathicus with its widespread congener Barbus barbus

In endemic species that co-occur with widespread congeners, hybridization can lead to an influx of novel and beneficial genetic variation, but high rates of introgression may cause genetic swamping of the endemic species and have detrimental effects on its survival potential. This study examines hybridization between sympatric populations of the Carpathian barbel Barbus carpathicus , a recently discovered cryptic species with a restricted range, and the widespread common barbel Barbus barbus . Based on six diagnostic allozyme loci, a microsatellite locus and mtDNA, hybrids were found to be present at multiple localities within the Vistula River drainage (Baltic Sea) as well as in the Tisza River system of the Danube River drainage (Black Sea). However, the numbers of hybrids were very low; four individuals of 230 fish sampled from the Vistula drainage. Bayesian assessment of their nuclear genotypes suggested that two hybrids in the Vistula drainage and nine in the Tisza system were F₁ generation, and one in the Vistula drainage and one in the Tisza system were backcrosses (BC) to B. barbus , while no F₂ or BC to B. carpathicus were detected. No hybrid carried B. carpathicus mtDNA and cytonuclear linkage disequilibria showed significant positive associations between hybrid genotypes and B. barbus mtDNA, suggesting unidirectionality in the interspecific mating with a disproportionate contribution of B. barbus mothers. Despite geographically broad occurrence of hybrids, these data provide evidence of strong constraints on hybridization in the native breeding habitats and the lack of introgression towards B. carpathicus .     

The evolution of postpairing male mate choice

An increasing number of empirical studies in animals have demonstrated male mate choice. However, little is known about the evolution of postpairing male choice, specifically which occurs by differential allocation of male parental care in response to female signals. We use a population genetic model to examine whether such postpairing male mate choice can evolve when males face a trade‐off between parental care and extra‐pair copulations (EPCs). Specifically, we assume that males allocate more effort to providing parental care when mated to preferred (signaling) females, but they are then unable to allocate additional effort to seek EPCs. We find that both male preference and female signaling can evolve in this situation, under certain conditions. First, this evolution requires a relatively large difference in parental investment between males mated to preferred versus nonpreferred females. Second, whether male choice and female signaling alleles become fixed in a population versus cycle in their frequencies depends on the additional fecundity benefits from EPCs that are gained by choosy males. Third, less costly female signals enable both signaling and choice alleles to evolve under more relaxed conditions. Our results also provide a new insight into the evolution of sexual conflict over parental care.     

CAN REINFORCEMENT COMPLETE SPECIATION?

Hybridization is common in nature, even between "good" species. This observation poses the question of why reinforcement is not always successful in leading to the evolution of complete reproductive isolation. To study this question, we developed a new "quasi-linkage disequilibrium" (QLD) approximation to obtain the first analytic results for the evolution of modifiers that increase mate discrimination against hybrids and heterospecifics. When such modifiers have small effects, they evolve more readily under a one-allele than a two-allele mechanism (sensu Felsenstein 1981). The strength of selection on the modifier decreases as hybrids decrease in frequency, and so further reinforcement may not occur once hybridization is sufficiently rare. The outcome is qualitatively different when modifiers have large effects, however, for example, when a single mutation can cause complete reproductive isolation. In this case, modifiers in a two-allele mechanism can be selected as or more strongly than those in a one-allele mechanism. Furthermore, they can spread under quite general conditions. Thus, whether complete closure of genetic introgression by reinforcement occurs may depend on the size of effects that mutations have on the sensory systems used in mate choice.     

Introgression of resistance genes between populations: a model study of insecticide resistance in Bemisia tabaci

Introgression is a key process in conservation biology, genetic modification of (crop) species and in the evolutionary ecology of many species. Here we consider the case of introgression of insecticide resistance in the whitefly, Bemisia tabaci. B. tabaci is a species complex consisting of a range of biotypes, known to have a high degree of inter-biotype reproductive isolation. In areas where insecticide resistant and susceptible biotypes of B. tabaci coexist, introgression of the resistance gene will have considerable consequences for whitefly control. Using a stochastic branching process model we calculate the relative importance of life-history traits in determining the probability of introgression given that a hybridization event has occurred. We show that a fitness cost expressed through the average number of eggs laid, has the largest effect on the introgression probability as compared to fitness costs expressed through other life-history parameters. These results change when we consider a reproductive isolation mechanism, for which we show that the fitness cost expressed through the male survival and mating probability have the largest effect on the probability of introgression.     

Relative abundance and the species-specific reinforcement of male mating preference in the Chrysochus (Coleoptera: Chrysomelidae) hybrid zone

Most studies of reinforcement have focused on the evolution of either female choice or male mating cues, following the long-held view in sexual selection theory that mating mistakes are typically more costly for females than for males. However, factors such as conspecific sperm precedence can buffer females against the cost of mating mistakes, suggesting that in some hybrid zones mating mistakes may be more costly for males than for females. Thus, the historical bias in reinforcement research may underestimate its frequency. In this study, we present evidence that reinforcement has driven the evolution of male choice in a hybrid zone between the highly promiscuous leaf beetles Chrysochus cobaltinus and C. auratus, the hybrids of which have extremely low fitness. In addition, there is evidence for male choice in these beetles and that male mating mistakes may be costly, due to reduced opportunities to mate with conspecific females. The present study combines laboratory and field methods to quantify the strength of sexual isolation, test the hypothesis of reproductive character displacement, and assess the link between relative abundance and the strength of selection against hybridization. We document that, while sexual isolation is weak, it is sufficient to produce positive assortative mating. In addition, reproductive character displacement was only detected in the relatively rare species. The strong postzygotic barriers in this system are sufficient to generate the bimodality that characterizes this hybrid zone, but the weak sexual isolation is not, calling into question whether strong prezygotic isolation is necessary for the maintenance of bimodality. Growing evidence that the cost of mating mistakes is sufficient to shape the evolution of male mate choice suggests that the reinforcement of male mate choice may prove to be a widespread occurrence.