Variation in female mate preference across a grasshopper hybrid zone

A method for studying variation in female preference among populations free from the confounding effects of variation in male characters is described. This method is applied to sixteen populations in a transect across a hybrid zone in the grasshopper, Chorthippus parallelus. Significant variation in preference is revealed among populations. The pattern of this variation is analysed in the context of the reinforcement model of speciation. While the data do indicate an increased homogamic preference on one side of the zone relative to more distant populations, this pattern cannot be distinguished statistically from an abrupt transition in preference over a distance of less than 1 km. We argue that either of these patterns implies that selection operates on female preferences in the hybrid zone.     

Maladaptive mate choice maintained by heterozygote advantage

Common buzzards (Buteo buteo) show a plumage polymorphism that appears to be maintained by heterozygote advantage and allows a maladaptive form of mate choice to persist. The light and dark morphs have a much lower fitness than the presumed heterozygous intermediate morph, but are replenished through Mendelian segregation in intermediate-intermediate pairs. Light and dark morphs could maximize their fitness by mating light with dark to produce all intermediate offspring, but instead choose partners of their own color, thereby producing broods of minimally fit homozygotes. Such maladaptive behavior argues forcefully against mate choice based on "good genes," and its persistence is best explained by heterozygote advantage maintaining the polymorphism coupled with nongenetic mate choice based on sexual imprinting. Modeling different patterns of mate choice shows that random mating and preference for own morph fit our data poorly, whereas preference for mother's morph yields a good fit.     

Hybrid female mate choice as a species isolating mechanism: environment matters

A fundamental goal of biology is to understand how new species arise and are maintained. Female mate choice is potentially critical to the speciation process: mate choice can prevent hybridization and thereby generate reproductive isolation between potentially interbreeding groups. Yet, in systems where hybridization occurs, mate choice by hybrid females might also play a key role in reproductive isolation by affecting hybrid fitness and contributing to patterns of gene flow between species. We evaluated whether hybrid mate choice behaviour could serve as such an isolating mechanism using spadefoot toad hybrids of Spea multiplicata and Spea bombifrons. We assessed the mate preferences of female hybrid spadefoot toads for sterile hybrid males vs. pure‐species males in two alternative habitat types in which spadefoots breed: deep or shallow water. We found that, in deep water, hybrid females preferred the calls of sterile hybrid males to those of S. multiplicata males. Thus, maladaptive hybrid mate preferences could serve as an isolating mechanism. However, in shallow water, the preference for hybrid male calls was not expressed. Moreover, hybrid females did not prefer hybrid calls to those of S. bombifrons in either environment. Because hybrid female mate choice was context‐dependent, its efficacy as a reproductive isolating mechanism will depend on both the environment in which females choose their mates as well as the relative frequencies of males in a given population. Thus, reproductive isolation between species, as well as habitat specific patterns of gene flow between species, might depend critically on the nature of hybrid mate preferences and the way in which they vary across environments.     

Assortative mating across a hybrid zone in Chorthippus parallelus (Orthoptera: Acrididae)

Two subspecies of the grasshopper Chorthippus parallelus meet and form a hybrid zone in the Pyrenees. Both strong hybrid dysfunction and a behavioural difference occur, which would seem to make the zone a suitable candidate for speciation by reinforcement. One of the classic ways of looking for this is to test for increased levels of assortative mating between populations from close to the region of contact. Here we show that, with virgin insects, such assortment decreases as one approaches the centre of the zone in C. parallelus. The pattern is different upon remating, with non-virgins showing a pattern more like that predicted by reinforcement. Overall there is little evidence for reinforcement. We argue that other tests of the model may be more appropriate for stable hybrid zones.     

Variation in female mate choice within guppy populations: population divergence,multiple ornaments and the maintenance of polymorphism

The evolutionary significance of variation in mate choice behaviour is currently a subject of some debate and considerable empirical study. Here, I review recent work on variation within and among guppy (Poecilia reticulata) populations in female mate choice and mating preferences. Empirical results demonstrate that there is substantial variation within and among populations in female responsiveness and choosiness, and much of this variation is genetic. Evidence for variation in preference functions also exists, but this appears to be more equivocal and the relative importance of genetic variation is less clear cut. In the second half of this review I discuss the potential significance of this variation to three important evolutionary issues: the presence of multiple male ornaments, the maintenance of polymorphism and divergence in mate recognition among populations. Studies of genetic variation in mate choice within populations indicate that females have complex, multivariate preferences that are able to evolve independently to some extent. These findings suggest that the presence of multiple male ornaments may be due to multiple female mating preferences. The extreme polymorphism in male guppy colour patterns demands explanation, yet no single satisfactory explanation has yet emerged. I review several old ideas and a few new ones in order to identify the most promising potential explanations for future empirical testing. Among these are negative frequency dependent selection, environmental heterogeneity coupled with gene flow, and genetic constraints. Last, I review the relative extent of within and among-population variation in mate choice and mating preferences in order to assess why guppies have not speciated despite a history of isolation and divergence. I argue that variation within guppy populations in mate choice and enhanced mating success of new immigrants to a pool are major impediments to population divergence of the magnitude that would be required for speciation to occur.     

Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet, and habitat choice

There has been considerable debate in the study of hybrid zones as to whether hybrids may be superior to parental types within the area of contact (bounded hybrid superiority). In birds, naturally occurring hybridization is relatively common, and hybridization within this group always involves mate choice. If hybrids are superior, females choosing heterospecific mates should be expected to show higher fitness under the conditions prevalent in the hybrid zone. Hybrid superiority under these circumstances would reduce reinforcement and thereby help to maintain the hybrid zone. To examine this issue, we studied reproductive performances of hybrids and parental species of gulls (Larus occidentalis and Larus glaucescens) at two colonies within a linear hybrid zone along the west coast of the United States. This hybrid zone contains predominantly gulls of intermediate phenotype. Previous studies indicated that hybrids were superior to one or both parental types, but provided no data on possible mechanisms that underlie this hybrid superiority. Using a hybrid index designed specifically for these species, we identified to phenotype more than 300 individuals associated with nests, including both individual males and females within 73 pairs in the central portion of the hybrid zone and 74 pairs in the northern portion of the hybrid zone. There was little evidence of assortative mating, and what little there was resulted solely because of pairings within intergrades. In the central hybrid zone, females paired with hybrid males produced larger clutches and hatched and fledged more chicks compared with females paired to western gull males. This was a result of heavy predation on eggs in sand habitat, where male western gulls established territories. In contrast, many hybrid males established territories in vegetated cover that was less vulnerable to predation. In the northern part of the hybrid zone, clutch size did not differ among pair categories, however, there were differences in hatching and fledging success, with females paired to hybrid males showing better success compared to females paired to glaucous-winged gull males. Hybrids showed better hatching and fledging success in the north because hybrids are more like western gulls than glaucous-winged gulls in foraging behavior, taking a higher percentage of fish in their diet, which enhances chick growth and survival. This is believed to be the first documentation of bounded hybrid superiority that delineates the mechanisms that underlie hybrid superiority.     

Microsatellite paternity analysis on captive Lake Malawi cichlids supports reproductive isolation by direct mate choice

Three sympatrically occurring members of a cichlid fish species complex from Lake Malawi have previously been reported to show assortative mating in the field. Offspring from three experimental tanks each housing both sexes of all three members of this complex were screened at one to four microsatellite loci to determine paternity. Reproductive isolation was found to persist without exception under laboratory conditions, providing strong evidence for behavioural barriers to mating. Direct mate choice is suggested as the process preventing interbreeding. The results are interpreted with reference to the rapid and explosive evolution of the cichlid group.     

Congruence between independent character systems across a hybrid zone: patterns in geographic space

The hybrid zone between eastern and western grass snakes, which has been independently hypothesized to be due to secondary contact, is investigated using univariate and multivariate analysis of a large number of independent, quantitative characters. Investigation of the patterns of geographic variation show that 5 out of 6 character systems show a congruent pattern of “stepped clinal” change across the zone. Insofar as this case is concerned, secondary contact ‘hybrid’ zones are associated with concordant changes in many character systems and “speciation” involves the origin of a large number of small differences in most character systems rather than the major reorganisation of a single system.     

Evolution of mate choice and the so‐called magic traits in ecological speciation

Non‐random mating provides multiple evolutionary benefits and can result in speciation. Biological organisms are characterised by a myriad of different traits, many of which can serve as mating cues. We consider multiple mechanisms of non‐random mating simultaneously within a unified modelling framework in an attempt to understand better which are more likely to evolve in natural populations going through the process of local adaptation and ecological speciation. We show that certain traits that are under direct natural selection are more likely to be co‐opted as mating cues, leading to the appearance of magic traits (i.e. phenotypic traits involved in both local adaptation and mating decisions). Multiple mechanisms of non‐random mating can interact so that trait co‐evolution enables the evolution of non‐random mating mechanisms that would not evolve alone. The presence of magic traits may suggest that ecological selection was acting during the origin of new species.     

UNDERSTANDING THE BASIS OF DIMINISHED GENE FLOW BETWEEN HYBRIDIZING CHROMOSOME RACES OF THE HOUSE MOUSE

Speciation may be promoted in hybrid zones if there is an interruption to gene flow between the hybridizing forms. For hybridizing chromosome races of the house mouse in Valtellina (Italy), distinguished by whole‐arm chromosomal rearrangements, previous studies have shown that there is greater interruption to gene flow at the centromeres of chromosomes that differ between the races than at distal regions of the same chromosome or at the centromeres of other chromosomes. Here, by increasing the number of markers along race‐specific chromosomes, we reveal a decay in between‐race genetic differentiation from the centromere to the distal telomere. For the first time, we use simulation models to investigate the possible role of recombination suppression and hybrid breakdown in generating this pattern. We also consider epistasis and selective sweeps as explanations for isolated chromosomal regions away from the centromere showing differentiation between the races. Hybrid breakdown alone is the simplest explanation for the decay in genetic differentiation with distance from the centromere. Robertsonian fusions/whole‐arm reciprocal translocations are common chromosomal rearrangements characterizing both closely related species and races within species, and this fine‐scale empirical analysis suggests that the unfitness associated with these rearrangements in the heterozygous state may contribute to the speciation process.     

Assortative mating,sexual selection,and their consequences for gene flow in Littorina

When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple-effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis, occur in North Atlantic rocky-shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size-assortative mating has previously been documented. Here, we analyze the mating pattern in L. saxatilis with respect to size in intensively sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment.     

No species barrier by call in an avian hybrid zone between California and Gambel's quail (Callipepla californica and C. gambelii)

Acoustic signals sometimes act as premating isolating barriers between animal species, but we know little about the circumstances that dictate the presence and strength of these barriers. Among insects, barriers to backcrossing are strengthened by acoustic signals that are under genetic control. Hybrid signals tend to be intermediate to parental signals, and signals are recognized only by like‐types, which results in reinforced species boundaries. This is not typically the case in avian taxa. Instead, acoustic signal transmission is controlled by some combination of genes and learning, and perhaps as a consequence of this variation, vocalizations play a diversity of roles in avian hybrid zones. I used California and Gambel's quail (Callipepla californica and C. gambelii), hybridizing birds that do not learn to vocalize, to explore whether genetically determined vocalizations function as a species barrier. Using spectral analysis, I measured temporal features of calls of uniquely colour‐banded quail that were recorded across one area of the California and Gambel's quail hybrid zone. Species discrimination is known to occur under captive conditions, though its basis is unexplored. Here I show that differences in the calls of parental species are likely great enough to permit species discrimination. Hybrid call components were intermediate to those of the parental species and covaried with genetic traits, as assessed with seven highly polymorphic microsatellite loci. Contrary to expectation, males as frequently called in response to unlike‐ as like‐type females who had initiated antiphonal calling, which is a courtship call between a female and a male. Furthermore, paired males and females did not share like‐type assembly calls, nor was there a correlation between the female's genetic or plumage traits and her mate's advertisement call. Based on these results, I conclude that California and Gambel's quail recognize each other and hybrids as potential mates and backcrossing occurs frequently. Thus, compatible mating signals could contribute to increased mixing of gene pools and slow the rate of speciation. I suggest that selection to respond to wide signal variation within species and imprinting on calls of mixed‐species coveys may cause mating signal compatibility between classes within the area of hybridization. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 253–264.     

Flower colour variation across a hybrid zone in Antirrhinum as perceived by bumblebee pollinators

To assess if pollinators’ behaviour could explain the maintenance of hybrid zones between different flower colour morphs, we analyzed flower colour variation in an Antirrhinum hybrid zone using spectrometry and a model of bee perception. Some colours generated by hybridization were not observed in any Antirrhinum species and even appeared to be rare among angiosperms. Variation in flower colours within the hybrid zone was continuous; the most similar colours were predicted not to be discriminated from one another in natural foraging situations. However, when compared at a scale corresponding to bees’ foraging range, some flower colours could be discriminated from all colours displayed by neighbouring plants. This could affect pollinator behaviour and explain lower visitation rates within the centre of the hybrid zone. Behavioural studies involving bumblebees and plant mixtures of parental and hybrid flower colours carefully characterized with appropriate visual models will be necessary to test this hypothesis. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Handling editor: Lars Chittka     

Discrete genetic variation in mate choice and a condition-dependent preference function in the side-blotched lizard: implications for the formation and maintenance of coadapted gene complexes

Variation in female preference functions, both genotypic andphenotypic, has been largely ignored in the literature, despiteits implications to the maintenance of genetic variation inpopulations and the resolution of the "Lek paradox." Polymorphicpopulations, such as in the side-blotched lizard, provide idealstudy systems for its investigation, especially in the contextof incipient processes of sympatric speciation. Females of theside blotch lizard exist in 2 genetically distinct morphs, yellowthroated and orange throated, that experience disruptive selectionfor life history traits. Males express 3 throat color morphs,blue, orange, and yellow, that exhibit alternative strategiesin intrasexual competition. We experimentally tested for femalepreference in triadic mate choice trials to identify the presenceof discrete genetic and condition-dependent variation in femalepreference function. We found that females did in fact showgenetic variation in preference for males but that females alsooperate a multicondition preference function dependent uponthe genotype of the female and her state (number of clutcheslaid). Females exhibited positive assortative mating prior tothe first clutch. However, prior to later clutches, orange femalesswitched choice, preferring yellow males. These findings arediscussed in relation to the maintenance of coadapted gene complexeswithin populations and the prevention of divergent directionalselection (population bifurcation) by condition-dependent variationin mate choice.     

Pre-mating isolation is determined by larval rearing substrates in cactophilicDrosophila mojavensis. II. Effects of larval substrates on time to copulation,mate choice and mating propensity

Summary It has been hypothesized that reproductive character displacement has evolved in mainland Sonora, Mexico populations of cactophilicD. mojavensis due to the presence of a sympatric sibling speciesD. arizonae. In laboratory tests using ancestral Baja California populations and derived, sympatric mainland populations, asymmetrical sexual isolation has been observed among populations ofD. mojavensis where mainland females discriminate against Baja males. Effects of different pre-adult rearing environments on adult mating behaviour were assessed by comparing fermenting cactus tissues like those used in nature for breeding with laboratory media because previous studies have employed synthetic growth media for fly growth and development. Significant behavioural isolation was evident in all cases when larvae were reared on laboratory food, but was non-significant when flies were reared on fermenting cactus, except for the cactus used by most mainland populations, consistent with previous studies. Time to copulation of Baja females was greater than mainland females over all substrates, but male time to copulation did not differ between populations. Time to copulation for both sexes was significantly greater when flies were reared on laboratory food with one exception. The degree of behavioural isolation was weakly correlated with time to copulation across food types (Spearman rank correlation = 0.58,p = 0.099). Therefore, use of laboratory media in this and previous studies exaggerated adult pre-mating isolation and time to copulation in comparison to natural breeding substrates. These experiments suggest that a change in host substrates by saprophagous insects (where chemical differences exist between hosts) may have subtle effects on mating behaviour in a manner which promotes low levels of sexual isolation as a by-product of their utilization of a particular substrate during larval development. ForD. mojavensis, these results suggest that over evolutionary time, radiation into a new environment (from Baja to the mainland) allowed utilization of new host plants that may have incidentally promoted the sexual isolation patterns that have been observed within this species.See Etges (1992) for the first paper in this series.     

Gene flow across a hybrid zone maintained by a weak heterogametic incompatibility and positive selection of incompatible alleles

Hybridization between incipient species is more likely to produce sterile or inviable F₁ offspring in the heterogametic (XY or ZW) sex than in the homogametic (XX or ZZ) sex, a phenomenon known as Haldane's rule. Population dynamics associated with Haldane's rule may play an important role in early speciation of sexually reproducing organisms. The dynamics of the hybrid zone maintained by incomplete hybrid inferiority (sterility/inviability) in the heterogametic sex (a ‘weak’ Haldane's rule) caused by a Bateson–Dobzhansky–Muller incompatibility was modelled. The influences and interplays of the strengths of incompatibility, dispersal, density‐dependent regulation (DDR) and local adaptation of incompatible alleles in a scenario of short‐range dispersal (the stepping‐stone model) were examined. It was found that a partial heterogametic hybrid incompatibility could efficiently impede gene flow and maintain characteristic clinal noncoincidence and discordance of alleles. Density‐dependent regulation appears to be an important factor affecting hybrid zone dynamics: it can effectively skew the effects of the partial incompatibility and dispersal as measured by effective dispersal, clinal structures and density depression. Unexpectedly, local adaptation of incompatible alleles in the parental populations, which would be critical for the establishment of the incompatibility, exerts little effect on hybrid zone dynamics. These results strongly support the plausibility of the adaptive origin of hybrid incompatibility and ecological speciation: an adaptive mutation, if it confers a marginal fitness advantage in the local population and happens to cause epistatic inferiority in hybrids, could efficiently drive further genetic divergence that may result in the gene becoming an evolutionary hotspot.