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.     

Contact Pheromones as Mate Recognition Cues of Four Species of Longhorned Beetles (Coleoptera: Cerambycidae)

We tested the hypothesis that contact phermones mediate mate recognition for four species of longhorned beetles, Neoclytus mucronatus mucronatus (F.), Megacyllene caryae (Gahan), Megacyllene robiniae (Forster), and Plectrodera scalator (F.). All tested males of all four species attempted to mate with females only after contacting them with their antennae. From 66.7 to 80% of tested males attempted to mate with hexane-extracted dead females treated with 0.1–1.0 female equivalents of conspecific female extracts, confirming that nonpolar compounds on the cuticle of females are essential for mate recognition in all four species. These findings are further evidence of the critical role of contact pheromones in mating systems of longhorned beetles.     

Males,but not females,perform strategic mate searching movements between host plants in a leaf beetle with scramble competition polygyny

Mate searching is assumed to be performed mostly by males, but when females benefit from multiple mating or are under risk of failing to mate, they may also perform mate searching. This is especially important in scramble competition polygynies, in which mate searching is the main mechanism of mate competition. Typically, more mobile individuals are expected to achieve higher mating success because mobility increases their probability of finding mates. If we assume individual movements are mainly explained by mate searching in scramble competition polygynies, we can investigate searching strategies by asking when individuals should leave their location and where they should go. We hypothesize that individuals will leave their locations when mating opportunities are scarce and will seek spatially close sites with better mating opportunities. We tested these hypotheses for males and females of Leptinotarsa undecimlineata, a leaf beetle with scramble competition polygyny in which both sexes are promiscuous. Individuals mate and feed exclusively on Solanum plants, and thus, individual movements can be described as switches between plants. Females were less likely than males to leave isolated plants, and both males and females moved preferentially to neighboring plants. Males were more likely to leave when the local number of females was low, and the number of males was high. They moved to plants with more females, a behavior consistent with a mate searching strategy. Females were more likely to move to plants with fewer males and many females, a behavior consistent with male harassment avoidance. Strategic movement is widely considered in foraging context, but seldom in a mate searching context. Considering that selection to minimize searching costs, maximize mating success, and minimize harassment may be ubiquitous in nature, we argue that strategic movements by mate searching individuals are likely to occur in many species.     

Model for genetic control of Heliothis virescens

Summary A model was developed which corrects and extends an earlier one proposed for the control of the tobacco budworm, Heliothis virescens (F.), through hybrid male sterility. Population suppression is effected through the release into natural populations of the backcross progeny of a hybrid between H. virescens and a related species. Thereafter, the system perpetuates itself in nature through continual backcrossing of the fertile backcross females to native H. virescens males. When the proportion of backcross hybrid females in the total population is large enough to draw off the insemination potential of the native males, the native females fail to replace themselves. The present model demonstrated that the ratio of released backcross hybrids to natural H. virescens remains constant in a closed population. Furthermore it was shown that the release ratio necessary to achieve extinction of a closed population is related to the number of females that a male can inseminate and to the population growth rate. Release ratios required to slow natural population growth and to lessen the impact damage of releases on crop plants were also examined. Effects of selection against the backcross females on the predictions of the model were explored.     

Chemically-mediated pre-mating behavior in two tetranychid species

We used bioassays to evaluate the arrestment response of male twospotted spider mite, Tetranychus urticae Koch, and Banks grass mite, Oligonychus pratensis (Banks) to whole-body extract from conspecific quiescent deutonymphs. We examined the effect of previous behavior on mite response to extract from female quiescent deutonymphs. We also examined male arrestment and guarding behavior in response to 2 extract concentrations and to extract from male quiescent deutonymphs. Male T. urticae and O. pratensis exhibited similar changes in their behavior in response to the different extracts with which we presented them. Males that were guarding quiescent deutonymphs immediately prior to testing spent more time in an untreated 3.5-mm-diameter circle than did males that were previously engaged in other behaviors. However, when nonguarding males were presented with extract of conspecific female quiescent deutonymphs they remained in the stimulus circle as long as guarding males did in an untreated circle. Arrestment duration of nonguarding males increased at 2 higher extract concentrations. The arrestment response was not exclusive to extracts from female quiescent deutonymphs; nonguarding male mites were also arrested by extracts from male quiescent deutonymphs, although for a shorter time. Duration of arrestment was related roughly to size differences between male and female quiescent deutonymphs. Furthermore, males did not show an exclusive preference for guarding conspecific male or female quiescent deutonymphs. It seems unlikely that the arrestant is a specific sex pheromone. Rather, male mites probably use the arrestant as a necessary cue to focus their attention on an individual that may be a suitable mate. Other tactile, visual, and chemical stimuli may then help males to decide whether to remain and assume mate guarding behaviors.     

Mating behavior of male deer ticksIxodes dammini (Acari: Ixodidae)

To analyze the sexual behavior of male black-legged deer ticks Ixodes dammini,we collected ticks infesting 202 white-tailed deer. On average, 17.7 males and 8.8 females infested each deer. Field-collected males copulated with a mean of 2.25 females, and virgin males mated with 2.4 females. On experimental hosts, males established sexual contact with feeding females and repelled other males, and about half remained paired after their mate detached. Engorged females continue to be receptive, and males mate more readily with them than with nonfed females. We conclude that male I. damminiare endowed with a repertoire of behaviors which favor an opportunistic mating before seeking a host and a preference for mating with feeding females on the host accompanied by tenacious mate guarding.     

Effects of density experience on mate guarding behavior by adult male Kanzawa spider mites

In the Kanzawa spider mite, Tetranychus kanzawai (Acari: Tetranychidae), adult males guard pre-reproductive quiescent females. I experimentally examined the effects of density experience during development and/or after adult emergence on precopulatory mate guarding behavior by T. kanzawai males. Mate guarding behavior was modified by density experience after adult emergence. When males had previously experienced high density after adult emergence (n = 71), 73.2% of them engaged in precopulatory mate guarding. In contrast, when males had previously experienced low density after adult emergence (n = 82), 61.0% of them did not guard females. Mate guarding with physical contact occurred more frequently when males had previously experienced a high density of potential rivals than when they had not, but the difference in behavior between the two groups of males was marginally not significant. Nevertheless, these results suggest overall that T. kanzawai males change mate guarding behavior in response to previously experienced density.     

拟环纹豹蛛雄蛛触肢上黑白相间毛饰物的功能

狼蛛科雄蛛附肢上多样化的饰装往往与求偶行为相偶联,这些特殊的饰装通常被认为是雌性选择的结果。拟环纹豹蛛Pardosa pseudoannulata,属狼蛛科豹蛛属,雄蛛触肢胫节密被白毛,跗舟密被黑毛,具有典型的性二型现象;同时,只有成熟的雄蛛才展现触肢黑白相间的毛饰物。推测拟环纹豹蛛雄蛛触肢这种黑白相间的毛饰物可能在物种识别中具重要作用。在室内我们拟通过涂抹操作对拟环纹豹蛛雄蛛触肢黑白相间毛饰物的功能进行分析。实验分为4组,分别是对照组(A组,雄蛛不做任何处理)、雄蛛触肢白色胫节全部涂成黑色(B组)、雄蛛触肢黑色跗舟全部涂成白色(C组)和雄蛛触肢的黑色跗舟被涂成黑色(D组),然后采用雌雄配对进行求偶交配行为测定。实验结果表明,B组雄蛛的交配成功率显著低于A、C和D组的雄蛛,而后3组雄蛛的交配成功率无显著差异。相反,B组雄蛛被雌蛛相食百分率显著高于其它3组。可见拟环纹豹蛛雄蛛触肢上黑白相间毛饰物,尤其是其胫节上的白色饰物在雌蛛种间识别中起重要作用。     

Behavioral reproductive isolation inDrosophila silvestris,D. heteroneura,and their F1 hybrids (Diptera: Drosophilidae)

We investigated the role that courtship and aggressive interactions may have for the maintenance of reproductive isolation betweenDrosophila silvestris andD. heteroneura. We examined the behavioral bases of reproductive isolation between the parental species and we examined the courtship success of each sex of both reciprocal F₁ hybrids when paired with the parental species. We found reduced copulation success among heterotypic parental pairs compared to homotypic pairs, which was primarily due to the lack of courtship initiation betweenD. silvestris males andD. heteroneura females. When hybrid males from both reciprocal crosses were paired with parental females their copulation successes were not significantly different from that of parental males. In contrast, hybrid females from both crosses had reduced copulation success withD. silvestris males, which in turn was primarily due to a reduced success of reaching later stages of courtship. The time spent in copulation by hybrid males was intermediate between the two parental males. We studied aggression by observing the interactions of males of heterotypic pairs, both between the parental species and between the hybrids and parental males. A lack of aggressive interactions betweenD. silvestris males andD. heteroneura males in addition to the lack of courtship suggests thatD. silvestris males do not respond toD. heteroneura individuals of either sex. Hybrid males were equally successful in winning fights with bothD. silvestris andD. heteroneura males. These results indicate that the behavioral isolation betweenD. silvestris andD. heteroneura may be largely a consequence of the earliest stages of interactions. The two species may differ either in activity levels or in morphological or chemical traits that are important for species and mate recognition. The relatively high copulation and aggressive success of hybrids indicates that sexual selection against hybrids alone is unlikely to be a sufficient force to reduce gene flow and maintain species distinctions.     

Functional rare males in diploid parthenogenetic Artemia

Functional males that are produced occasionally in some asexual taxa – called ‘rare males’ – raise considerable evolutionary interest, as they might be involved in the origin of new parthenogenetic lineages. Diploid parthenogenetic Artemia produce rare males, which may retain the ability to mate with females of related sexual lineages. Here, we (i) describe the frequency of male progeny in populations of diploid parthenogenetic Artemia, (ii) characterize rare males morphologically, (iii) assess their reproductive role, using cross‐mating experiments with sexual females of related species from Central Asia and characterize the F1 hybrid offspring viability and (iv) confirm genetically both the identity and functionality of rare males using DNA barcoding and microsatellite loci. Our result suggests that these males may have an evolutionary role through genetic exchange with related sexual species and that diploid parthenogenetic Artemia is a good model system to investigate the evolutionary transitions between sexual species and parthenogenetic strains.     

MECHANISMS OF FEMALE CHOICE IN RED JUNGLE FOWL

We examined mate preference behavior in red jungle fowl, Gallus gallus, to determine if the mechanism of mate preference used by females was relative or absolute. Under a relative model, females compare males and prefer the one with the most exaggerated form of secondary sex character, regardless of where the proffered males lie along the population distribution of the trait. Under an absolute or threshold model, females have a threshold for the character, above which they will exert a preference and below which they will not. Female red jungle fowl preferred roosters with longer combs and redder irises, but this preference was exerted only when hens mated quickly; females mating slowly mated at random. The threshold model was supported in two ways: i) chosen males from the fast-mating group had larger combs than chosen males in the slow-mating group; ii) when the same female was presented with two pairs of males in two different trials, one large-combed pair and one small-combed pair, hens mated significantly more slowly, and often refused to mate, when only short-combed roosters were available. Hens thus alter their behavior depending on the males they see, and they may not exert a preference at all if both males fall below the threshold. Further corroborating evidence comes from a set of mate choice trials using underdeveloped roosters, in which males had small combs and females mated slowly or did not mate. The method of choice used by females could affect the speed with which correlations develop between the genes for male traits and genes for female preferences. Sexual selection for good genes may be more consistent with an absolute than a relative method of female choice.     

Adaptive control of copulation duration by males under sperm competition in the mite,Macrocheles muscaedomesticae

In a manure-inhabiting predatory mite, Macrocheles muscaedomesticae (Gamasida, Macrochelidae), when the female mates with two males, the first male takes nearly perfect fertilization priority (Yasui, 1988). The present study examined whether the first-male's sperm precedence is influenced by the copula-duration of the first and second males mating with the same female, and whether males control their copulation duration by assessing the probability that the mate has been inseminated by other males. Results of the artificial interruption of copulation showed that sperm precedence value, P₂ (the proportion of the offspring fathered by the second male), was negatively correlated with the copulation duration of the first male but positively correlated with that of the second male. There was a threshold (ca. 180–300 seconds) in the first-male's copulation duration beyond which P₂ decreased drastically; when length of the first copulation exceeded this threshold, the second males did not fertilize eggs, whereas they fertilized more than half of the eggs when the first-copulation duration was shorter than the threshold. Almost all males copulated for a longer period (average 509.8 seconds) than this threshold if the copulation duration of the previous male had not exceeded the threshold, but if it was longer than the threshold, second males had shortened their copulation (67.6 seconds). These results suggest that males are able to assess the insemination status of their mates and to adjust their copulation duration depending on the probability of fertilizing eggs by their own sperm. A mechanistic explanation for sperm precedence (i.e., plug-formation within sperm receptive organ of the females) is proposed.     

The evolution of autosomal suppressors of sex-ratio drive in Drosophila simulans

Sex-ratio drive, which results in males siring female-biased progeny, has been reported in several Drosophila species, including D. simulans. It is caused by X-linked drivers that prevent the production of Y-bearing sperm. In natural populations of D. simulans, the drivers are usually cryptic, because their spread has elicited the evolution of drive suppressors. We investigated autosomal suppression in flies from Madagascar, Réunion and Kenya. Autosomal suppressors were found in all three places, indicating that they are a regular component of drive suppression over this geographic area, where strong Y-linked suppressors also occur. These suppressors were suspected of being polymorphic in Madagascar and Réunion and proved to be polymorphic in Kenya. We developed a model simulating the evolution of neutral autosomal suppressors in order to explore the effects of the number of suppressor genes, their relative strength and the co-occurrence of Y-linked suppressors. The most interesting prediction of the model is that when suppression is multigenic, suppressor loci can remain polymorphic despite the absence of balancing selection if an equal sex-ratio is restored in the population before the suppressor alleles become fixed at all loci. The model also emphasises the importance of the sterility of distorters sons in suppressor dynamics.     

Dispersal and mating structure of a parasitoid with a female-biased sex ratio: Implications for theory

Summary Species of parasitic Hymenoptera that manifest female-biased sex ratios and whose offspring mate only with the offspring of the natal patch are assumed to have evolved biased sex ratios because of Local Mate Competition (LMC). Off-patch matings, i.e. outcrossing, are inconsistent with the conditions favouring biased sex ratios because they foster a mating structure approaching panmixia. Such a mating structure favours parents who invest equally in daughters and sons, assuming the production of each sex is of equal cost.Pachycrepoideus vindemiae (Rondani) is a solitary pupal parasitoid of patchily distributed frugivorousDrosophila, whose offspring manifest a female-biased sex ratio. Thus this species appears to manifest a population structure and progeny sex ratio consistent with LMC. However, preliminary observations and subsequent greenhouse experiments suggest that the males participate in off-patch matings and that this propensity is unlikely to be an experimental artefact. FemaleP. vindemiae dispersed from patches in which either the males were lacking (12% of the emigrant females), both resident (sibling) and immigrant males were present (23% of the females), only immigrant males were present (14% of the females), or their opportunity to mate could not be determined (14% of the females). Of the 12% that emigrated from a patch lacking males, an estimated 7% mated at an oviposition site and 5% remained unmated, presumably because they arrived at an oviposition site that lacked males before they were dissected to determine whether they were inseminated. Thus the degree of bias in the sex ratios of the progeny (18% males), coupled with the suggested outcrossing potential from the experiments (26–37%), is inconsistent with the assumptions of LMC or variants of it, i.e. asynchronous brood maturation. Thus the explanation for a biased sex ratio in the offspring ofP. vindemiae remains a conundrum. More importantly,P. vindemiae does not appear to be an isolated example.     

Video Playback Versus Live Stimuli for Assessing Mate Choice in a Pipefish

Synopsis In this study, I investigated the application of the video playback technique to studies on mate choice in the pipefish, Syngnathus typhle. In this sex-role reversed species, the males are predominately the choosing sex, and given a choice, prefer to mate with larger females. As such, I tested if this known mate preference remained when using this novel experimental technique. Specifically, I compared the response of males to video images of females to that of live females. Results revealed that male pipefish showed a stronger preference for the larger female in the video playback treatment than in the clear glass (two-way interaction) live female treatment. This experiment has, therefore, demonstrated that the pipefish respond in the predicted direction in response to video playback, and as such proves to be a reliable method to study mate preferences in this species.     

Behavior of male and female spruce bark beetles,Ips typographus,on the bark of host trees during mass attack

The behavior of 118 spruce bark beetles, Ips typographus,was observed on trees under colonization. Most individuals were followed from when they landed until they entered or left the tree. Both males and females spent most time inspecting crevices and searching for a place to start boring or for a hole to enter. These behaviors accounted for 87 and 70% of all behavioral acts recorded for males and females, respectively. Females entered galleries with males only after a period of pushing at the gallery entrance. Males spent on average 3 min and females 4 min on the bark before entering or leaving the tree. Thirty-three percent of the beetles eventually entered the tree, 31% flew away, 35% dropped from the host, and one beetle was eaten by a predator. The results are discussed in relation to the question of mate choice in bark beetles and to studies on attack dynamics of spruce bark beetle populations.     

Triploid females and diploid males: underreported phenomena in <Emphasis Type="Italic">Polistes</Emphasis> wasps?

Summary In hymenopteran species, males are usually haploid and females diploid. However, in species that have complementary sex determination (CSD), diploid males arise when a female produces offspring that are homozygous at the sex-determining locus. Although diploid males are often sterile, in some species they have been shown to produce diploid sperm, thus producing triploid daughters if they mate successfully. Diploid males have been observed in very few species of social wasps, and we know of no published reports of triploid females. In this paper, we review the existing literature on diploid males and triploid females in the Hymenoptera, and report the observation of triploid females in three species of Polistes paper wasps. Although polyploid offspring may be produced parthenogenetically, the more likely scenario is that Polistes wasps have CSD and produce diploid males via homozygosity at the sex-determining locus. Therefore, female triploidy indicates that diploid males do exist in Polistes species where they are presumed to be absent, and are likely to be even more frequent among species that have experienced a genetic bottleneck. We conclude by cautioning against the assumption of a selective advantage to the production of early males, and by discussing the implications of male diploidy and female triploidy for measurement of sex ratio investment and assumptions of reproductive skew theory.Received 5 December 2003; revised 20 March 2004; accepted 19 April 2004.     

Male mate choice in the Andrew’s toad <Emphasis Type="Italic">Bufo andrewsi</Emphasis>: a preference for larger females

In amphibians, theory predicts that male mate choice with respect to female body size can be expected to occur when female fecundity is related to body size and when the time and energy invested into one mating are relatively large. Based on experimental observations, we tested whether male mate choice occurs in a population of the Andrew’s toad (Bufo andrewsi), a species in which both assumptions are likely to be met. When a male B. andrewsi was placed with a gravid female and a non-gravid similar-sized female, the male did not discriminate between them. When two gravid females with distinct size differences were provided to a male, the male preferred the larger one. In an experiment in which two different-sized gravid females were put in two separate transparent cylinders to exclude potential chemical cues, males spent more time in proximity to the larger gravid females and jumped more frequently towards the larger gravid females than the smaller ones. These findings suggest that male B. andrewsi recognizes female body size, exhibits mate choice, and prefers to mate with larger females that provide greater reproductive potential.     

Assortative mating among Anastrepha fraterculus (Diptera: Tephritidae) hybrids as a possible route to radiation of the fraterculus cryptic species complex

Reproductive isolation among populations of Anastrepha fraterculus has been found acting at the pre‐ and post‐zygotic levels. Differences in timing of sexual activity and male sexual pheromone composition among populations could partially account for prezygotic isolation. Hybrid males were found to produce a novel pheromone, which is a mix of parental pheromones. In the present study, we found that the hybrid females showed a significant preference to mate with hybrid males than with parental males. Male location during pheromone emission is associated with its reproductive success and, thus, differences in the location of males during courtship could also play a role in isolation. We found evidence that reproductive isolation is also related to the location of males during courtship. Hybrid male behaviour regarding location during pheromone release was found to be influenced by the maternal lineage. If these populations hybridized in the field, the hybrid females would tend to mate with hybrid males probably leading to the formation of a new entity within the A. fraterculus complex. This simple and fast process could be one reason explaining the high number of taxonomic entities within this complex. Further studies on other members of the fraterculus species group may reveal whether this can be considered as an example of homoploid hybrid speciation. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 346–354.     

同种雄性竞争对手的存在对星豹蛛雄蛛求偶和交配行为的影响

越来越多的研究发现,雄性产生精子(精液)也需付出代价。雄性除了依据配偶质量和竞争对手的竞争强度适应性调整生殖投入外,雄性在求偶和交配行为上也相应产生适应性反应,求偶和交配行为具有可塑性。目前雄性求偶和交配行为可塑性研究主要集中于雌性多次交配的类群中,在雌性单次交配的类群中研究甚少。以雌蛛一生只交配一次而雄蛛可多次交配的星豹蛛为研究对象,比较:(1)前一雄性拖丝上信息物质对后续雄蛛求偶和交配行为的影响,(2)雌雄不同性比对雄蛛求偶和交配行为的影响。研究结果表明,星豹蛛前一雄蛛拖丝上的信息物质对后续雄蛛求偶潜伏期、求偶持续时间和交配持续时间都没有显著影响,但前一雄蛛拖丝上的信息物质对后续雄蛛求偶强度有显著抑制作用。同时,性比对星豹蛛雄蛛求偶和交配行为都没有显著影响。可见,星豹蛛雄蛛对同种雄性拖丝上的化学信息可产生求偶行为的适应性调整,而对性比不产生适应性反应。