Mating Discrimination Research Articles

Sex-specific discrimination of familiar and unfamiliar mates in the Tokay gecko

Social animals need to keep track of other individuals in their group to be able to adjust their behaviour accordingly and facilitate group cohesion. This recognition ability varies across species and is influenced by cognitive capacities such as learning and memory. In reptiles, particularly Squamates (lizards, snakes, and worm lizards), chemical communication is pivotal for territoriality, reproduction, and other social interactions. However, the cognitive processes underlying these social interactions remain understudied. In our study, we examined the ability of male and female Tokay geckos (Gekko gecko) to chemically differentiate familiar and unfamiliar mating partners. Our findings suggest that both sexes can make this distinction, with males responding more to the odour of a familiar mate, and females responding more to unfamiliar mates. The lizards maintained their discriminatory abilities for two to three weeks but not up to six weeks after separation. This research highlights the efficacy of using odours as social stimuli for investigating social cognition in lizards, a promising avenue to better understand social cognition in these animals.

Mate Discrimination Using Chemical Cues by Male Guppies.

Males often perform mate choice with the aim of maximizing reproductive success. To identify profitable mates, the males of some animals are known to use visual and chemical cues derived from females. In this study, we aimed to examine mate discrimination by male guppies (Poecilia reticulata) using chemical cues received from females under different reproductive statuses, i.e., virgin females, pregnant females, females after copulation with another male, and post-partum females. We conducted a dichotomous choice experiment for each combination of chemical stimuli from females under different reproductive statuses. In experiment 1, in which females were removed from water that was subsequently used as a chemical stimulus, male preferences did not differ significantly in all combinations of chemical stimuli from females under different reproductive statuses. However, in experiment 2, in which females remained within bottles containing the water used as a chemical stimulus, with the exception of one combination of chemical stimuli, significant differences in male preferences were detected for chemical stimuli derived from females under different reproductive statuses. Overall, males generally showed a preference for chemical stimulus received from females after copulation with other males. The findings of this study indicate that male guppies can discriminate the reproductive status of females based solely on chemical cues that may disappear or degenerate within a short period of time, thereby facilitating profitable mate choice.

Mate Discrimination of Colocasiomyia xenalocasiae and C. alocasiae (Diptera: Drosophilidae) as a Possible Factor Contributing to their Co-Existence on the Same Host Plant

Mate Discrimination of Colocasiomyia xenalocasiae and C. alocasiae (Diptera: Drosophilidae) as a Possible Factor Contributing to their Co-Existence on the Same Host Plant

Virus infection modulates male sexual behaviour in Caenorhabditis elegans.

Mating dynamics follow from natural selection on mate choice and individuals maximizing their reproductive success. Mate discrimination reveals itself by a plethora of behaviours and morphological characteristics, each of which can be affected by pathogens. A key question is how pathogens affect mate choice and outcrossing behaviour. Here we investigated the effect of Orsay virus on the mating dynamics of the androdiecious (male and hermaphrodite) nematode Caenorhabditis elegans. We tested genetically distinct strains and found that viral susceptibility differed between sexes in a genotype‐dependent manner with males of reference strain N2 being more resistant than hermaphrodites. Males displayed a constitutively higher expression of intracellular pathogen response (IPR) genes, whereas the antiviral RNAi response did not have increased activity in males. Subsequent monitoring of sex ratios over 10 generations revealed that viral presence can change mating dynamics in isogenic populations. Sexual attraction assays showed that males preferred mating with uninfected rather than infected hermaphrodites. Together our results illustrate for the first time that viral infection can significantly affect male mating choice and suggest altered mating dynamics as a novel cause benefitting outcrossing under pathogenic stress conditions in C. elegans.

Mate discrimination among subspecies through a conserved olfactory pathway.

Communication mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active, male-specific pheromones. One functions as a conserved male antiaphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in combination with auditory signals. Unexpectedly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically, and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in Drosophila melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection, and interpretation do not necessarily evolve in a coordinated manner.

Experimental Introgression To Evaluate the Impact of Sex Specific Traits on Drosophila melanogaster Incipient Speciation.

Sex specific traits are involved in speciation but it is difficult to determine whether their variation initiates or reinforces sexual isolation. In some insects, speciation depends of the rapid change of expression in desaturase genes coding for sex pheromones. Two closely related desaturase genes are involved in Drosophila melanogaster pheromonal communication: desat1 affects both the production and the reception of sex pheromones while desat2 is involved in their production in flies of Zimbabwe populations. There is a strong asymmetric sexual isolation between Zimbabwe populations and all other “Cosmopolitan” populations: Zimbabwe females rarely copulate with Cosmopolitan males whereas Zimbabwe males readily copulate with all females. All populations express desat1 but only Zimbabwe strains show high desat2 expression. To evaluate the impact of sex pheromones, female receptivity and desat expression on the incipient speciation process between Zimbabwe and Cosmopolitan populations, we introgressed the Zimbabwe genome into a Cosmopolitan genome labeled with the white mutation, using a multi-generation procedure. The association between these sex-specific traits was determined during the procedure. The production of pheromones was largely dissociated between the sexes. The copulation frequency (but not latency) was highly correlated with the female—but not with the male—principal pheromones. We finally obtained two stable white lines showing Zimbabwe-like sex pheromones, copulation discrimination and desat expression. Our study indicates that the variation of sex pheromones and mating discrimination depend of distinct—yet overlapping—sets of genes in each sex suggesting that their cumulated effects participate to reinforce the speciation process.

Speciation: On the Scent of Mate Discrimination Genes

Animals use smell to recognize individuals from their own species and find suitable mates. A study of female chemical cues in two species of fruit flies uses a creative genetic strategy to identify an allele that is involved in species recognition and may play an important role in keeping these species apart in nature.

Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species.

Mate discrimination is a key mechanism restricting gene flow between species. While studied extensively with respect to female mate choice, mechanisms of male mate choice between species are far less studied. Thus, we have little knowledge of the relative frequency, importance, or overall contribution of male mate discrimination to reproductive isolation. In the present study, we estimated the relative contributions of male and female choice to reproductive isolation between Drosophila simulans and D. sechellia, and show that male mate discrimination accounts for the majority of the current isolation between these species. We further demonstrate that males discriminate based on female cuticular hydrocarbon pheromones, and collect evidence supporting the hypothesis that male mate discrimination may alleviate the costs associated with heterospecific courtship and mating. Our findings highlight the potentially significant contribution of male mate choice to the formation of reproductive isolating barriers, and thus the speciation process.

Development of Novel Polymorphic EST-SSR Markers in Bailinggu (Pleurotus tuoliensis) for Crossbreeding.

Identification of monokaryons and their mating types and discrimination of hybrid offspring are key steps for the crossbreeding of Pleurotus tuoliensis (Bailinggu). However, conventional crossbreeding methods are troublesome and time consuming. Using RNA-seq technology, we developed new expressed sequence tag-simple sequence repeat (EST-SSR) markers for Bailinggu to easily and rapidly identify monokaryons and their mating types, genetic diversity and hybrid offspring. We identified 1110 potential EST-based SSR loci from a newly-sequenced Bailinggu transcriptome and then randomly selected 100 EST-SSRs for further validation. Results showed that 39, 43 and 34 novel EST-SSR markers successfully identified monokaryons from their parent dikaryons, differentiated two different mating types and discriminated F1 and F2 hybrid offspring, respectively. Furthermore, a total of 86 alleles were detected in 37 monokaryons using 18 highly informative EST-SSRs. The observed number of alleles per locus ranged from three to seven. Cluster analysis revealed that these monokaryons have a relatively high level of genetic diversity. Transfer rates of the EST-SSRs in the monokaryons of closely-related species Pleurotus eryngii var. ferulae and Pleurotus ostreatus were 72% and 64%, respectively. Therefore, our study provides new SSR markers and an efficient method to enhance the crossbreeding of Bailinggu and closely-related species.

Modelling of Yeast Mating Reveals Robustness Strategies for Cell-Cell Interactions.

Mating of budding yeast cells is a model system for studying cell-cell interactions. Haploid yeast cells secrete mating pheromones that are sensed by the partner which responds by growing a mating projection toward the source. The two projections meet and fuse to form the diploid. Successful mating relies on precise coordination of dynamic extracellular signals, signaling pathways, and cell shape changes in a noisy background. It remains elusive how cells mate accurately and efficiently in a natural multi-cell environment. Here we present the first stochastic model of multiple mating cells whose morphologies are driven by pheromone gradients and intracellular signals. Our novel computational framework encompassed a moving boundary method for modeling both a-cells and α-cells and their cell shape changes, the extracellular diffusion of mating pheromones dynamically coupled with cell polarization, and both external and internal noise. Quantification of mating efficiency was developed and tested for different model parameters. Computer simulations revealed important robustness strategies for mating in the presence of noise. These strategies included the polarized secretion of pheromone, the presence of the α-factor protease Bar1, and the regulation of sensing sensitivity; all were consistent with data in the literature. In addition, we investigated mating discrimination, the ability of an a-cell to distinguish between α-cells either making or not making α-factor, and mating competition, in which multiple a-cells compete to mate with one α-cell. Our simulations were consistent with previous experimental results. Moreover, we performed a combination of simulations and experiments to estimate the diffusion rate of the pheromone a-factor. In summary, we constructed a framework for simulating yeast mating with multiple cells in a noisy environment, and used this framework to reproduce mating behaviors and to identify strategies for robust cell-cell interactions.

Characterization of assortative mating in medaka: Mate discrimination cues and factors that bias sexual preference

Somatolactin alpha (SLα) is a peptide hormone that regulates skin color, and SLα-deficient and SLα-excess strains have been established in medaka (Oryzias latipes). Their skin colors differ conspicuously and males prefer to mate with females from the same strain. Pre-mating sexual isolation in this model vertebrate provides an ideal platform for investigating the molecular mechanisms of mate choice. Thus, we studied the sensory cues utilized by these fish to discriminate the same and different strains. When males were given a choice under monochromatic light, where the skin colors differed only in terms of brightness but not in hue, mating occurred but it was not assortative. This suggests that: (1) a visual cue is essential for mate discrimination rather than odor or acoustic cues; (2) the visual cue is color and not shape, size, or motion; and (3) the color cue needs to be perceived as the relative balance of brightness at multiple wavelengths rather than the brightness at a specific wavelength. In addition, we introduced another skin-color mutation into the SLα-excess strain and found that this new strain and the original SLα-excess strain, which also overexpressed SLα but exhibited distinct skin colors, preferred different colors. This demonstrates that SLα is not a primary determinant of sexual preference. The symmetrically biased sexual preferences of the SLα-deficient and SLα-excess strains may be acquired postnatally depending on their individual skin color or that of tank mates.

Sexual selection and incipient speciation in Hawaiian Drosophila

We conducted sexual selection experiments to produce strains with high and low mating discrimination in females of laboratory strains of Hawaiian Drosophila, D. silvestris, then examined secondary sexual traits of these two lines, and compared them with that of standard line. In order to do this, we screened out super-males which mated successfully with females and with high mating records; and poor males which usually could not mate successfully with females and had low mating records. In the meantime, choosy females were also screened out, which almost never responded to males’ nuptial dance and were difficult to be mated; but indiscriminate females were on the contrary, which were very ready to accept male’s nuptial dance and were very easy to be mated. As a result, by mating super-males with choosy females, we were able to produce the high-line strain; similarly, for the low line, we mated poor males with indiscriminate females and we had a strain that was significantly different from our standard strain within just two generations of selection, i.e., morphological trait differences were measured between the standard strain and the two selected lines, which indicated that mating discrimination has affected secondary sexual traits of the low-line strain significantly: Cilia number on the foretibia of low-line males is significantly different from that of the standard line, which perhaps was the indication of incipient speciation in Hawaiian Drosophila.

Multimodal Chemosensory Circuits Controlling Male Courtship in Drosophila

Throughout the animal kingdom, internal states generate long-lasting and self-perpetuating chains of behavior. In Drosophila, males instinctively pursue females with a lengthy and elaborate courtship ritual triggered by activation of sexually dimorphic P1 interneurons. Gustatory pheromones are thought to activate P1 neurons but the circuit mechanisms that dictate their sensory responses to gate entry into courtship remain unknown. Here, we use circuit mapping and in vivo functional imaging techniques to trace gustatory and olfactory pheromone circuits to their point of convergence onto P1 neurons and reveal how their combined input underlies selective tuning to appropriate sexual partners. We identify inhibition, even in response to courtship-promoting pheromones, as a key circuit element that tunes and tempers P1 neuron activity. Our results suggest a circuit mechanism in which balanced excitation and inhibition underlie discrimination of prospective mates and stringently regulate the transition to courtship in Drosophila.

Pheromone-Mediated Mate Location and Discrimination by Two Syntopic Sibling Species of Dendroctonus Bark Beetles in Chiapas, Mexico.

Where their geographic and host ranges overlap, sibling species of tree-killing bark beetles may simultaneously attack and reproduce on the same hosts. However, sustainability of these potentially mutually beneficial associations demands effective prezygotic reproductive isolation mechanisms between the interacting species. The pine bark beetle, Dendroctonus frontalis Zimmermann, is syntopic in the Central American region with a recently described sibling species, Dendroctonus mesoamericanus Armendáriz-Toledano and Sullivan, but mechanisms for their reproductive isolation are uncertain. We investigated whether semiochemicals mediate species discrimination by mate-seeking males of both species. In olfactometer bioassays, walking males of both species strongly preferred odors from gallery entrances of conspecific females. Coupled gas chromatography-electroantennographic detection and gas chromatography-mass spectrometry isolated 16 olfactory stimulants for males in these odors, but only two, ipsdienol and endo-brevicomin (both from D. mesoamericanus females), differed in quantity in female-associated odors between the species. In olfactometer bioassays, with 10, 1, or 0.1 female entranceequivalents of synthetic semiochemicals, the combination of ipsdienol and endo-brevicomin inhibited responses of male D. frontalis and enhanced responses of male D. mesoamericanus to two compounds associated with female entrances of both species (the pheromone component frontalin and host odor α-pinene). We conclude that ipsdienol and endo-brevicomin, pheromone components produced by females of just one of the two species (D. mesoamericanus), mediate interspecific mate discrimination by males of both species and provide an apparently symmetrical reproductive isolation mechanism.

Confrontation of cryptic diversity and mate discrimination within Gammarus pulex and Gammarus fossarum species complexes

Summary Freshwater amphipods Gammarus fossarum and Gammarus pulex are widespread in Europe, with some evidence of cryptic diversity in the former. We used DNA barcoding to assess genetic diversity within and among amphipod populations and examined mate discrimination and pre‐copulatory pair formation between genetically divergent individuals. Eight distinct G. fossarum and four distinct G. pulex molecular operational taxonomic units (MOTUs) were detected. Among the 33 amphipod populations sampled, 11 contained a single MOTU, 11 had two and 11 were composed of three sympatric MOTUs. Genetic divergences between sympatric MOTUs (G. fossarum and G. pulex MOTUs combined) ranged up to 28% (Kimura two parameter estimates). In amphipod populations containing sympatric MOTUs, pre‐copulatory pair formation was random between MOTUs diverging by <4%. However, pre‐copulatory pairs involving amphipod individuals from MOTUs diverging by >4% were rare, suggesting mate discrimination between sympatric, highly divergent MOTUs. Although the likelihood decreased with genetic distance between partners, pre‐copulatory pair formation in the laboratory can occur between MOTUs diverging by c. 16% and led to successful mating: most female amphipod carried viable, fertilised eggs 48 h post‐mating. Data showed high cryptic diversity in the G. fossarum/G. pulex groups, even at a small spatial scale. Mate discrimination between genetically divergent amphipods in natural populations suggests that some of the MOTUs found in G. fossarum and G. pulex may be separated into (sub)species. However, amphipods from different MOTUs can still form pre‐copulatory pairs and females produce viable eggs. Overall, data suggest that cryptic diversity is common in the G. fossarum/G. pulex groups and that pre‐zygotic isolation through mate discrimination, rather than post‐zygotic incompatibility, is likely to drive cryptic speciation.

Discrimination of mates and intruders: visual and olfactory cues for a monogamous territorial coral reef butterflyfish

Recognition of conspecifics is essential for territorial and monogamous animals in order to maintain pair bonds, mate-guard and defend territories. However, cues required for mate discrimination are essentially unknown in monogamous fishes, despite the importance of recognition behaviour that promotes this mating system. This field study tested the role of visual and olfactory cues in the discrimination of mates and unfamiliar conspecifics in the territorial, socially monogamous pebbled butterflyfish, Chaetodon multicinctus. A series of model bottle field experiments presented cues from a mate and an unfamiliar nonmate to a focal resident fish within its feeding territory. When both visual and olfactory cues were first matched, the resident spent more time and engaged in more agonistic displays near the bottled intruder. In contrast, when olfactory cues of bottled fish were first mismatched, the resident fish spent equivalent time at each bottle stimulus. When scent cues were then reversed to a matched odour condition (odour released next to bottled fish), the resident again spent more time with the nonmate. Resident fish spent equivalent time with the mate and nonmate in the absence of any associated odour stimuli. In addition, resident fish did not show a differential response when the mate's odour was associated with only one of two intruder fish. Thus both visual and olfactory cues are necessary for butterflyfish to discriminate their mate from intruders within feeding territories. These results indicate that mate recognition in animals with long-term pair bonds may require multimodal stimuli and future studies on mate recognition should address multiple sensory channels.

ON THE COYNE AND ORR-IGIN OF SPECIES: EFFECTS OF INTRINSIC POSTZYGOTIC ISOLATION, ECOLOGICAL DIFFERENTIATION, X CHROMOSOME SIZE, AND SYMPATRY ONDROSOPHILASPECIATION

Coyne and Orr found that mating discrimination (premating isolation) evolves much faster between sympatric than allopatric Drosophila species pairs. Their meta-analyses established that this pattern, expected under reinforcement, is common and that Haldane's rule is ubiquitous in Drosophila species divergence. We examine three possible contributors to the reinforcement pattern: intrinsic postzygotic isolation, dichotomized as to whether hybrid males show complete inviability/sterility; host-plant divergence, as a surrogate for extrinsic postzygotic isolation; and X chromosome size, whether roughly 20% or 40% of the genome is X-linked. We focus on "young" species pairs with overlapping ranges, contrasted with allopatric pairs. Using alternative criteria for "sympatry" and tests that compare either level of prezygotic isolation in sympatry or frequency of sympatry, we find no statistically significant effects associated with X chromosome size or our coarse quantifications of intrinsic postzygotic isolation or ecological differentiation. Although sympatric speciation seems very rare in animals, the pervasiveness of the reinforcement pattern and the commonness of range overlap for close relatives indicate that speciation in Drosophila is often not purely allopatric. It remains to determine whether increased premating isolation with sympatry results from secondary contact versus parapatric speciation and what drives this pattern.

Impact of mating behaviour on the success of malaria control through a single inundative release of transgenic mosquitoes

Transgenic mosquitoes are a potential tool for the control or eradication of insect-vectored diseases. For malaria, one possible strategy relies on the introduction of malaria-refractory transgenes into wild Anopheles mosquito populations that would limit their capacity to transmit the disease. The success of such an approach obviously depends on a variety of factors. By developing a model that integrates both population genetics and epidemiology, we explore how mosquito mating preferences and the cost and efficacy of refractoriness affects the long-term prevalence of malaria in humans subsequent to a single generation inundative release of male transgenic mosquitoes. As may be intuitively expected, mating discrimination by wild-type individuals against transgenic ones generally reduces the probability that transgenes become stably established at a high frequency in mosquito populations. We also show that in circumstances where transgenic individuals exhibit some degree of discrimination against wild-type individuals, this can favour the spread of refractory alleles and lead to a significant reduction in malaria prevalence in the human population (if the efficacy of a dominant refractory mechanism exceeds at least 75%). The existence of such a non-intuitive outcome highlights the practical value of increasing the understanding of Anopheles mating preferences in the wild as a means to harness them in the implementation of population replacement approaches. Potential strategies by which previously described mating preferences of Anopheles gambiae populations could be exploited to manipulate the mate choice of transgenic release stocks are discussed.

Genome differentiation of Drosophila melanogaster from a microclimate contrast in Evolution Canyon, Israel.

The opposite slopes of "Evolution Canyon" in Israel have served as a natural model system of adaptation to a microclimate contrast. Long-term studies of Drosophila melanogaster populations inhabiting the canyon have exhibited significant interslope divergence in thermal and drought stress resistance, candidate genes, mobile elements, habitat choice, mating discrimination, and wing-shape variation, all despite close physical proximity of the contrasting habitats, as well as substantial interslope migration. To examine patterns of genetic differentiation at the genome-wide level, we used high coverage sequencing of the flies' genomes. A total of 572 genes were significantly different in allele frequency between the slopes, 106 out of which were associated with 74 significantly overrepresented gene ontology (GO) terms, particularly so with response to stimulus and developmental and reproductive processes, thus corroborating previous observations of interslope divergence in stress response, life history, and mating functions. There were at least 37 chromosomal "islands" of interslope divergence and low sequence polymorphism, plausible signatures of selective sweeps, more abundant in flies derived from one (north-facing) of the slopes. Positive correlation between local recombination rate and the level of nucleotide polymorphism was also found.

Evolution of pre‐zygotic and post‐zygotic barriers to gene flow among three cryptic species within the Anastrepha fraterculus complex

AbstractTropical tephritids are ideally suited for studies on population divergence and speciation because they include species groups undergoing rapid radiation, in which morphologically cryptic species and sister species are abundant. The fraterculus species group in the Neotropical genus Anastrepha is a case in point, as it is composed of a complex of up to seven A. fraterculus morphotypes proposed to be cryptic species. Here, we document pre‐ and post‐zygotic barriers to gene flow among adults of the Mexican A. fraterculus morphotype and three populations (Argentina, Brazil, and Peru) belonging to two separate morphotypes (Brazilian 1 and Peruvian). We unveiled three forms of pre‐zygotic reproductive isolation resulting in strong assortative mating. In field cages, free‐ranging male and female A. fraterculus displayed a strong tendency to form couples with members of the opposite sex belonging to their own morphotype, suggesting that male pheromone emission, courtship displays, or both intervene in shaping female choice before actual contact and coupling. In addition, males and females of the Peruvian morphotype became receptive and mated significantly later than adults of the Mexican and Brazilian 1 morphotypes. After contact, Mexican females exhibited greater mating discrimination than males when facing adults of the opposite sex belonging to either the Peruvian or the Brazilian 1 morphotype as evidenced by vigorous resistance to penetration once they had been forcefully mounted by heterotypic males. Forced copulations resulted in production of F1 hybrids that were either less viable (and partially fertile) than parental crosses or even sterile. Our results suggest that the Mexican morphotype is a distinct biological entity and that pre‐zygotic reproductive isolation through divergence in courtship or male‐produced pheromone and other mechanisms appear to evolve faster than post‐zygotic isolation in the fraterculus species group.