Sex Differences in Mate Preference Between Two Hybridizing Species of Poeciliid Fish

When hybridization between two species in secondary contact is costly, natural selection should favor pre‐mating isolation barriers. The invasive Gambusia affinis has been introduced to habitats of a closely related species, the endangered Gambusia nobilis. Although other Gambusia species readily hybridize in secondary contact, previous studies in this system found low abundance of hybrids in sympatry. To examine whether hybridization is limited by behavioral pre‐mating isolation that may have evolved in allopatry, I examined each species’ mating preferences using individuals from allopatric populations in male and female visual/olfactory association preference tests as well as open mating tests with and without male–male competition. Gambusia affinis and G. nobilis males had significant association preference for conspecific females in visual/olfactory tests. Only G. nobilis females had statistically significant preference for conspecific males. In open mating tests, males of both species had lower chase times overall when in competition, but there was no difference in number of copulation attempts. Males of both species had higher copulatory success rates with conspecific females when in competition, suggesting females may exert some control over copulation success of males. These results suggest that there are differences in mating preferences between these species. This mate choice may act as a pre‐mating isolating barrier to reduce hybridization in sympatry, a proposed threat to the endangered G. nobilis.     

Influence of male courtship intensity and male–male competition on paternity distribution in Hermann's tortoise,Testudo hermanni hermanni (Chelonia: Testudinidae)

Honest‐advertisement models of sexual selection suggest that condition‐dependent male secondary sexual characters could function as reliable signals of male quality, enabling females to discriminate among potential partners, both in the pre‐ and post‐copulatory phases. In this context, many studies have revealed the importance of promiscuous mating systems and female sperm storage in determining the occurrence of such a model of sexual selection. By contrast, few studies have investigated the presence and extent of post‐copulatory female choice in chelonian species. The present study aimed to investigate the effect of male size, male–male competition, and courtship intensity on paternity distribution in Testudo hermanni hermanni, combining behavioural and genetic data. We created experimental groups composed of two males of different sizes and three or four randomly selected females. Observations conducted during social interactions between males revealed that a hierarchy, unrelated to male size, was soon established: Alpha males were more aggressive towards competitors and courted females more intensively. Alpha males also achieved a higher mounting success than Beta males. Paternity analysis performed on hatchlings produced from experimental females revealed that male reproductive success was not correlated with male–female size ratio. Finally, despite the higher mounting success of Alpha males, paternity analysis revealed that male reproductive success did not differ between Alpha and Beta males. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 656–667.     

Interspecific interactions and learning variability jointly drive geographic differences in mate preferences

Co‐occurrence of closely related species can cause behavioral interference in mating and increase hybridization risk. Theoretically, this could lead to the evolution of more species‐specific mate preferences and sexual signaling traits. Alternatively, females can learn to reject heterospecific males, to avoid male sexual interference from closely related species. Such learned mate discrimination could also affect conspecific mate preferences if females generalize from between species differences to prefer more species‐specific mating signals. Female damselflies of the banded demoiselle (Calopteryx splendens) learn to reject heterospecific males of the beautiful demoiselle (C. virgo) through direct premating interactions. These two species co‐occur in a geographic mosaic of sympatric and microallopatric populations. Whereas C. virgo males have fully melanized wings, male C. splendens wings are partly melanized. We show that C. splendens females in sympatry with C. virgo prefer smaller male wing patches in conspecific males after learning to reject heterospecific males. In contrast, allopatric C. splendens females with experimentally induced experience with C. virgo males did not discriminate against larger male wing patches. Wing patch size might indicate conspecific male quality in allopatry. Co‐occurrence with C. virgo therefore causes females to prefer conspecific male traits that are more species specific, contributing to population divergence and geographic variation in female mate preferences.     

Pre‐ and postcopulatory sexual selection act in concert to determine male reproductive success in Tribolium castaneum

To capture how sexual selection shapes male reproductive success across different stages of reproduction in Tribolium castaneum (Coleoptera, Tenebrionidae), we combined sequential sperm defence (P1) and sperm offence (P2) trials with additional trials where both males were added simultaneously to the female. We found a positive correlation between the relative paternity share in simultaneous male–male competition trials and the P2 trial. This suggests that males preferred by females as sires achieve superior fertilization success during sperm competition in the second male position. In simultaneous male–male competition trials, where pre‐, peri‐ and postcopulatory sexual selection were all allowed to act, the relative paternity share of preferred males was more than 20% higher than in P2 sperm competition trials where precopulatory female choice was disabled. Additional behavioural observations revealed that mating with more attractive males resulted significantly more frequently in offspring production than mating with less attractive males. Thus, by comparing male fertilization success in trials where precopulatory choice was turned off with more inclusive estimates of fertilization success where pre‐ and pericopulatory choice could occur, we show that female mate choice may effectively inhibit sperm competition. Female mate choice and sperm competition (P2) are positively correlated, which is consistent with directional sexual selection in this species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 67–75.     

Pre‐ and post‐mating reproductive barriers drive divergence of five sympatric species of Naryciinae moths (Lepidoptera: Psychidae)

The biological species concept suggests that species can be separated on the basis of reproductive isolation. However, because natural interbreeding capabilities are often unknown, differences in morphology are generally used to separate species. Alternatively, genetic dissimilarity is used to separate morphologically similar species. Many genetic markers, including the maternally inherited mitochondrial cytochrome oxidase I sequence, cannot show interbreeding and therefore species status of groups may remain unresolved. In species of the genera Dahlica and Siederia (Lepidoptera: Psychidae: Naryciinae) the lack of morphological distinction and unknown interbreeding has led to unclear and unresolved taxonomic status. Mitochondrial DNA sequences suggest five sexual species to occur in Finland. However, their species status remains unconfirmed, due to a lack of knowledge on interbreeding, unclear morphological distinction and the limited variation in mitochondrial DNA. We combine three methods, a cross‐mating experiment, an analysis of mitochondrial and nuclear DNA, and a detailed male genital morphological examination, to establish the species status of the five suspected species. All suspected species exhibit intraspecies mating preference, although several interspecies pairs readily produce offspring. The genetic analysis, however, fails to show hybrids or introgression, suggesting that both pre‐ and post‐copulation mechanisms isolate the species reproductively. Morphological analysis of the male genitalia confirms that the species have diverged. Our results highlight the need of combining behavioural, morphological and genetic methods to determine species status in challenging taxonomic groups. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 584–605.     

A role for ecology in male mate discrimination of immigrant females in Calopteryx damselflies?

Sexual selection against immigrants is a mechanism that can regulate premating isolation between populations but, so far, few field studies have examined whether males can discriminate between immigrant and resident females. Males of the damselfly Calopteryx splendens show mate preferences and are able to force pre‐copulatory tandems. We related male mate responses to the ecological characteristics of female origin, geographic distances between populations, and morphological traits of females to identify factors influencing male mate discrimination. Significant heterogeneity between populations in male mate responses towards females was found. In some populations, males discriminated strongly against immigrant females, whereas the pattern was reversed or nonsignificant in other populations. Immigrant females were particularly attractive to males when they came from populations with similar predation pressures and densities of conspecifics. By contrast, immigrant females from populations with strongly dissimilar predation pressures and conspecific densities were not attractive to males. Differences in the abiotic environment appeared to affect mating success to a lesser degree. This suggests that male mate discrimination is context‐dependent and influenced by ecological differences between populations, a key prediction of ecological speciation theory. The results obtained in the present study suggest that gene‐flow is facilitated between ecologically similar populations. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 506–518.     

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.     

Specialized visual learning of facial signals of quality in the paper wasp,Polistes dominula

Some primates and one species of paper wasp recognize faces using specific processing strategies to extract individual identity information from conspecific faces. Explanations for the evolution of face specialization typically focus on the complexity associated with individual recognition because all currently identified species with face specialization use faces for individual recognition. In the present study, we show an independent evolution of face specialization in a paper wasp species with facial patterns that signal quality rather than individual identity. Quality signals are simpler to process than individual identity signals because quality signals do not require simultaneous integration across multiple stimuli or learning and memory. Therefore, the results of the present study suggest that the complexity of processing may not be the key factor favouring the evolution of specialization. Instead, the predictable location of socially important signals relative to other anatomical features may allow easy categorization of features, thereby favouring specialized visual processing. Given that visual quality signals are found in many taxa, specific‐processing mechanisms for social signals may be widespread. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 992–997.     

Sexually Dimorphic Intrasexual Duetting in an Otherwise Monomorphic Green Lacewing (Neuroptera, Chrysopidae, Chrysoperla plorabunda): Sexual Selection or Sex Recognition?

Songs produced during heterosexual duets in a green lacewing, C. plorabunda, are sexually monomorphic. However, individuals of either sex will also engage in intrasexual duets, which can exhibit sexual dimorphism. We confined males and females together in various combinations in a small arena to study the phenotypes, behavioral interactions, and functional roles of duetting in this species. The goal was to test whether sexual selection or sex recognition provided the better explanation of song sexual dimorphism. We determined that the monomorphic form of the intrasexual duet was long and stable, and could take place either between males or between females. Such “standard” intrasexual duetting songs were acoustically indistinguishable from heterosexual songs. However, males could also engage other males in special “fast duets” that sped up and terminated abruptly. Equivalent fast duets were not part of the female repertory. Fast duetting songs between males differed significantly from other types of male or female duetting songs in every measurable characteristic, but their role in the mating system was ambiguous. Contrary to one prediction of the sexual selection hypothesis, fast duetting between males occurred less often in situations where it might be the most useful to males in securing mates, i.e., during male-male-female interactions (trios). In addition, fast songs that started, ended, both started and ended, or neither started nor ended duets were acoustically indistinguishable, making it unlikely that females were choosing males based on such variation. However, songs that “both started and ended” fast duets were associated with a significant mating advantage, indicating a possible role for fast duetting in male-male sexual competition. Because the alternative hypothesis of sex recognition was also supported by some of our results, we conclude that aggressive qualities of male-male fast duets probably mediate intrasexual selection, while their increasing tempo serves as an adaptive response to promote rapid sex recognition by truncating unproductive and potentially dangerous intrasexual duetting.     

Mate Choice by Both Sexes Maintains Reproductive Isolation in a Species Flock of Pupfish (Cyprinodon spp) in the Bahamas

Female and male mate choices can reinforce reproductive isolation after sympatric speciation. Using a binary choice design, we examine the importance of visual cues in female mate choice in all three sympatric species of pupfish on San Salvador Island. We also examine the importance of olfactory cues in female choice of the hard‐shelled invertebrate specialist (Cyprinodon brontotheroides). We examine male mate choice in two of the three species, the scale eater (C. desquamator) and the detritivore (C. variegatus). Females of all three species use visual cues and prefer conspecific males. C. brontotheroides females do not use olfactory cues to discriminate between conspecific and heterospecific males. Males of C. desquamator and C. variegatus also preferentially court conspecific females. Thus, mutual mate choice, where both females and males exhibit mate choice, acts as a strong behavioral pre‐mating isolation mechanism in these sympatrically speciated pupfish.     

Divergence in Female Duetting Signals in the Enchenopa binotata Species Complex of Treehoppers (Hemiptera: Membracidae)

Sexual communication often involves signal exchanges between the sexes, or duetting, in which mate choice is expressed through response signals. With both sexes acting as signalers and receivers, variation in the signals of males and females may be important for mate choice, reproductive isolation, and divergence. In the Enchenopa binotata species complex – a case study of sympatric speciation in which vibrational duetting may have an important role – male signals are species‐specific, females choose among males on the basis of signal traits that reflect species and individual differences, and female preferences have exerted divergent selection on male signals. Here, we describe variation in female signals in the E. binotata species complex. We report substantial species differences in the spectral and temporal features of female signals, and in their timing relative to male signals. These differences were similar in range to differences in male signals in the E. binotata complex. We consider processes that might contribute to divergence in female signals, and suggest that signal evolution in the E. binotata complex may be influenced by mate choice in both sexes.     

Male adaptations to minimize sexual cannibalism during reproduction in the funnel‐web spider Hololena curta

Males of many spider species risk being attacked and cannibalized while searching for, courting, and mating with conspecific females. However, there are exceptions. We show that the funnel‐web spider, Hololena curta, has 3 adaptations that minimize risk to males during courtship and mating, and enhance reproductive success. First, males detected chemical or tactile signals associated with webs of virgin females, and differentiated them from webs of mated females, enabling males to increase encounter rates with virgin females and avoid aggressive mated females. Second, males produced stereotyped vibrational signals during courting which induced female quiescence and suppressed female aggression. Third, when touched by males, sexually receptive females entered a cataleptic state, allowing males to safely approach and copulate. Because males can mate multiple times and the sex ratio in natural populations of H. curta is female biased, overall reproductive output is likely increased by males of this species avoiding sexual cannibalism.     

The flexible lek: Phymatopus hecta the gold swift demonstrates the evolution of leking and male swarming via a hotspot (Lepidoptera: Hepialidae)

Leking moths present an evolutionary problem in their apparently simultaneous reversal of male–female attraction. The mating system of Phymatopus (or Hepialus) hecta embraces an unusually wide range of procedures. Both males and females use medium‐range olfactory attractants (also probably visual signals), and both sexes will lure, and both will approach, the other, either when flying or perched. This produces an ‘infinite variety’ which includes the classic moth mating procedure (males fly to sessile female); a typical lek procedure (female flies to sessile male); a mating swarm (hovering male follows passing female); and intermediates such as a mutual courtship dance. Male behaviour includes a flying display, two sessile displays, and an escalating war of attrition. The system is versatile, persistent, and probably evolutionarily stable. The lek site has a high density of perches suitable for copulation which facilitate predator‐escape by means of a dead drop. The whole supports a model for the evolution of resource‐based leks which commence with a concentration of females on a hotspot, leading to a concentration of males; and then an escalating process of sexual selection as males become increasingly attractive over a distance to females, and females use the males as a way of locating the resource. The main stabilizing pressure may be selection for efficient mate acquisition, and as with grouse leking systems, the precondition for evolution was probably having travelling females that actively sought a reproductive resource or a predator free space. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 184–201.     

Effects of mating order and male size on embryo survival in a pipefish

In species that provide parental care, individuals should invest adaptively in their offspring in relation to the pre‐ and post‐zygotic care provided by their partners. In the broad‐nosed pipefish, Syngnathus typhle L., females transfer large, nutrient‐rich eggs into the male brood pouch during mating. The male broods and nourishes the embryos for several weeks before independent juveniles emerge at parturition. Given a choice, females clearly prefer large partners. Yet, females provide protein‐richer eggs when the same individual mates with a smaller than a larger male. In the present study, we allowed each female to mate with one small and one large male, in alternated order. We found a strong effect of female mating order, with larger clutches and higher embryo mortality in first‐ than second‐laid broods, which may suggest that eggs over‐ripen in the ovaries or reflect the negative effects of high embryo density in the brood pouch. In either case, this effect should put constraints on the possibility of a female being selective in mate choice. We also found that small and large males produced embryos of similar size and survival, consistent with the reproductive compensation hypothesis, suggesting that, in this species, larger males provide better nourishment to the embryos than smaller males. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 639–645.     

Reproductive interference between Aedes albopictus and Aedes flavopictus at a place of their origin

Aedes (Stegomyia) albopictus and Aedes (Stegomyia) flavopictus are related species that have overlapping distributions from southern to central Japan. To understand how they interact, we studied reproductive interference between them, particularly focusing on the body size difference between the mating pair. Here, we examined the effects of conspecific, heterospecific and double mating (i.e. heterospecific mating followed by conspecific mating) on copulation duration, egg production and hatchability of eggs using mosquitoes that varied in body size. Females mated only with heterospecific males produced few viable eggs, indicating that post‐mating isolation is almost complete. When mated with heterospecific males before conspecific mating, the production of viable eggs was lower than when mated only with conspecific males, revealing the occurrence of reproductive interference. The degree of reproductive interference was larger in Ae. flavopictus than in Ae. albopictus when the female size was small but did not differ between them when the female size was large. Aedes albopictus females appear to be able to distinguish Ae. flavopictus males from conspecific males and larger females are more successful in the rejection of heterospecific males. On the other hand, Ae. flavopictus were not able to discriminate between conspecific and heterospecific males.     

Consequences of genetic incompatibility on fitness and mate choice: the male point of view

Hymenopterans under single‐locus complementary sex determination (sl‐CSD) face inbreeding costs due to this sex determination mode. Under sl‐CSD, homozygote eggs at the sl‐CSD locus usually develop into unviable or sterile diploid males. Production of such costly males increases when sib‐mating happens because related individuals share half of their genome. In the hymenopteran Venturia canescens (a solitary parasitoid wasp), diploid males are sterile, leading to fitness costs through genetic incompatibility between parents. Whereas the costs of producing diploid males and behavioural strategies that would reduce such costs have been studied in females, the potential fitness costs faced by males have not. Here, we aimed to investigate fitness costs that males endure after a single sib‐mating and tested whether they have the ability to avoid sib‐mating through kin recognition. Our results show that males have a reduced fitness (i.e. they produce fewer daughters) when mating with their sibs. We also show that males have the ability to distinguish between non‐sib and sib females (i.e. kin). They use chemical marks emitted by the females to discriminate kin from non‐kin. We discuss the evolution of kin recognition in males in the context of mate choice for genetic compatibility. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 279–286.     

Male–male interactions and male mating success in the leafhopper Aphrodes makarovi

In mating systems based on substrate‐borne vibrations, sexual communication often involves a reciprocal exchange of species‐ and sex‐specific vibrational signals and male is searching for a stationary female. In the leafhopper Aphrodes makarovi, female reply is essential for successful location of the female and its variable duration directly affects male's costs associated with signalling and searching. We studied male and female behaviour in a trio situation (two males and one female), and our results show that male–male competition had important effects on male mating success. Females replied equally to advertisement calls emitted by the winning and losing males and mated with the first male that located them, regardless of his investment in calling effort. Males eavesdropped to male–female duet maintained by the rival, and the winners were better at exploiting female replies to the rival's advertisement calls by silently approaching the female. To interfere with the ongoing male–female duet, males also emitted masking signals overlapping the latter part of the female reply. More overlapped female replies were registered in response to the losers and masking signals most likely delay the rival in reaching the female. Our study shows that a comprehensive understanding of male mating success and female preferences in vibrational duetting systems requires also investigations in more complex settings that more realistically represent the situation in nature.     

Functional morphology of the visual system and mating strategies in bumblebees (Hymenoptera,Apidae, Bombus)

Bumblebee mating behaviour intrigued Darwin over 150 years ago and has elicited much interest since. Despite our increasing knowledge about male mating strategies, we still know little about the signals and cues involved, the sender‐receiver relationship and the functional adaptations of the involved sensory systems. Although several authors have noticed a close relationship between the mating system and male‐specific elaboration of the visual system, studies on the functional adaptations have yet to be conducted. We investigated the functional morphology of the compound eyes in 11 species of Bombus from various subgenera in detail. Of these, four species (Bombus confusus, Bombus melaleucus, Bombus mendax, Bombus niveatus) have enlarged male eyes, characterized by a higher number of ommatidia compared with worker eyes and a frontal zone with enlarged facets, which is likely to be associated with improved spatial resolution and contrast sensitivity. In these species, perching mating strategies are found. In contrast, males of species that patrol scent routes (Bombus hortorum, Bombus lapidarius, Bombus pascuorum, Bombus pratorum, Bombus soroeensis, Bombus terrestris, Bombus wurflenii) show no distinct eye adaptations, and their eye morphology closely resembles that of the workers. A phylogenetic analysis of male eye structure indicates that enlarged males eyes may have been the ancestral state in Bombus. © 2014 The Linnean Society of London     

Widespread reliance on olfactory sex and species identification by lyssomanine and spartaeine jumping spiders

Jumping spiders (Salticidae) are renowned for their exceptional vision, but this does not preclude use of other senses. Here we provide evidence that olfactory pheromones are widespread in the Spartaeinae and Lyssomaninae, two subfamilies regarded as basal clades within the Salticidae. Pheromone use by salticids was tested in a series of experiments: males were tested with the odour of conspecific females, heterospecific females, and conspecific males, and females were tested with the odour of conspecific males. With seven of the 29 species tested, we also tested males using the draglines of conspecific females (spider absent) as the odour source. Males of all species tested were attracted to the odour of conspecific females and to the odour of the draglines of conspecific females. There was no evidence of males responding to the odour of heterospecific females or conspecific males, or of females responding to the odour of conspecific males. These findings suggest that it is primarily males that respond to olfactory sex pheromones, consistent with the apparent trend within spiders of males more actively searching for females and females placing greater emphasis on mate‐choice decisions. Compared with most salticid groups, lyssomanines and spartaeines are unusually sedentary and this lifestyle may favour olfactory mate searching. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 664–677.