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Mate choice evolution, dominance effects, and the maintenance of genetic variation.

Female mate choice influences the maintenance of genetic variation by altering the mating success of males with different genotypes. The evolution of preferences themselves, on the other hand, depends on genetic variation present in the population. Few models have tracked this feedback between a choice gene and its effects on genetic variation, in particular when genes that determine offspring viability and attractiveness have dominance effects. Here we build a population genetic model that allows comparing the evolution of various choice rules in a single framework. We first consider preferences for good genes and show that focused preferences for homozygotes evolve more easily than broad preferences, which allow heterozygous males high mating success too. This occurs despite better maintenance of genetic diversity in the latter scenario, and we discuss why empirical findings of superior mating success of heterozygous males consequently do not immediately lead to a better understanding of the lek paradox. Our results thus suggest that the mechanisms that help maintain genetic diversity also have a flipside of making female choice an inaccurate means of producing the desired kind of offspring. We then consider preferences for heterozygosity per se, and show that these evolve only under very special conditions. Choice for compatible genotypes can evolve but its selective advantage diminishes quickly due to frequency-dependent selection. Finally, we show that our model reproduces earlier results on selfing, when the female choice strategy produces assortative mating. Overall, our model indicates that various forms of heterozygote-favouring (or variable) female choice pose a problem for the theory of sexual ornamentation based on indirect benefits, rather than a solution.

Animals↗

Role of the striatum and nucleus accumbens in paced copulatory behavior in the female rat.

Female rats engage in a series of approach and avoidance behaviors (pacing behavior) directed at the male in order to achieve a preferred rate of intromissions that make pregnancy more likely to occur with insemination. The striatum and nucleus accumbens have been implicated in the modulation of pacing behavior. It is unclear, however, whether these areas of the brain are necessary for the display of pacing behavior. To address this question, ovariectomized female rats received either bilateral quinolinic acid lesions of the striatum or nucleus accumbens or sham surgeries. After hormone priming, rats were allowed to engage in mating behaviors in an apparatus in which they could pace the rate of the copulatory bout. There was a significant reduction in pacing efficiency after striatal lesions, in that females were less likely to leave the male's side of the chamber after a contact. Animals with lesions of the nucleus accumbens that included the shell were more likely to avoid sexual interaction altogether than animals with control lesions. Therefore, it is concluded that the striatum and nucleus accumbens modulate specific aspects of pacing behavior in the female rat.

Animals↗

The indole alkaloid tryptamine impairs reproduction in Drosophila melanogaster.

The plant-produced indole alkaloid tryptamine is one of a large array of neuroactive substances that may affect insect behavior, development, and physiology. We tested the role of tryptamine on insect reproduction using the fruit fly, Drosophila melanogaster (Meigen), as a model system. Measurements were made of reproductive success, oviposition rate, and preadult survival of insects on artificial diets containing tryptamine, its precursor tryptophan, as well as glycine and serotonin (5-hydroxytryptamine). Drosophila reproduction was reduced to 15% of controls when adult insects mated and the young were allowed to develop on medium containing 75 mM tryptamine. Tryptamine-induced depression in reproductive success was due to decreased oviposition rate and preadult survival. Serotonin, but not tryptophan or glycine, also reduced oviposition rate. Preference tests indicated that tryptamine may act as an antiattractant or antifeedant in this species. The accumulation of the indole alkaloid tryptamine in plants may provide a mechanism for reducing insect reproduction, which is potentially useful in protecting crop plants.

Animals↗

Analysis of specific adaptation to a domicile habitat: a comparative study of two closely related cockroach species.

The German cockroach, Blattella germanica (L.), and the closely related species B. bisignata (Brunner) belong to the germanica species group. They are similar in appearance, life history, reproductive cycle, and courtship behavior. The most significant difference is habitat preferences: B. germanica is a household species and lives in crowded conditions, whereas the feral B. bisignata lives outdoors in a solitary manner. Nevertheless, B. bisignata has recently been found in households. A comparison between the two species has shown that B. germanica displays gregarious behavior and produces an aggregation pheromone, whereas both characters are absent in B. bisignata. Mate preference experiments have revealed that B. germanica females accepted only conspecific males, whereas B. bisignata females mated with males from both species, provided that long distance calling was bypassed. In addition, the high reproductive potential of B. germanica outcompeted the other species: when 10 pairs of B. germanica and of B. bisignata were kept together in crowded conditions during 3 mo, B. bisignata was driven into extinction. It is concluded that the chances of B. bisignata becoming a new household species are remote.

Adaptation, Physiological↗

Male phenotype predicts insemination success in guppies.

Theory predicts that mate choice can lead to an increase in female fecundity if the secondary sexual traits used by females to assess male quality covary with the number of sperm transferred during copulation. Where females mate multiply, such a relationship between male attractiveness and ejaculate size may, additionally (or alternatively), serve to augment the effect of indirect selection by biasing paternity in favour of preferred males. In either case, a positive correlation between male attractiveness and the size of ejaculates delivered at copulation is predicted. To date, some of the most convincing (indirect) evidence for this prediction comes from the guppy, a species of fish exhibiting a resource-free mating system in which attractive males tend to have larger sperm reserves. We show that, during solicited copulations, male guppies with preferred phenotypes actually transfer more sperm to females than their less-ornamented counterparts, irrespective of the size of their initial sperm stores. Our results also reveal that, during coercive copulations, the relationship between ejaculate size and the male's phenotype breaks down. This latter result, in conjunction with our finding that mating speed--a factor under the female's control-is a significant predictor of ejaculate size, leads us to speculate that females may exert at least partial control over the number of sperm inseminated during cooperative matings.

Animals↗

Male mate choice selects for female coloration in a fish.

Although sexual selection theory has proved successful in explaining a wide array of male ornaments, the function of ornaments occurring in females is largely unknown. Traditionally, female ornaments have been considered nonfunctional, being merely a genetically correlated response to selection for male ornamentation. However, this hypothesis is only relevant to species in which the ornament is basically the same in the two sexes. Alternatively, female ornaments may be influenced by selection acting directly on the females, either through female-female competition or male choice. We tested the latter hypothesis in mate-choice experiments with two-spotted gobies (Gobiusculus flavescens). In this small marine fish, females have bright yellow-orange bellies during the breeding season, a conspicuous trait that is not present in males. We conducted two aquarium experiments to test whether males preferred to mate with more colorful females. In the first experiment, males had a choice between two females that varied in natural coloration (and belly roundness). In the second experiment, we manipulated belly coloration and kept roundness constant. Males spent more time with colorful than with drab females in both experiments and also performed far more courtship displays toward colorful females. Our study provides experimental evidence that males prefer ornamented females in a fish that is not sex-role reversed, supporting the hypothesis that female ornamentation is sexually selected.

Animals↗

Call duration as an indicator of genetic quality in male gray tree frogs.

The "good genes" hypothesis predicts that mating preferences enable females to select mates of superior genetic quality. The genetic consequences of the preference shown by female gray tree frogs for long-duration calls were evaluated by comparing the performance of maternal half-siblings sired by males with different call durations. Offspring of male gray tree frogs that produced long calls showed better performance during larval and juvenile stages than did offspring of males that produced short calls. These data suggest that call duration can function as a reliable indicator of heritable genetic quality.

Animals↗

Comparison of puncture versus vasotomy techniques for vasography in an animal model.

PURPOSE: We determine the adverse effects of 2 different techniques of vasography in an animal model. MATERIALS AND METHODS: Unilateral vasography was performed by a direct puncture technique with a lymphangiogram needle or through a partial thickness vasostomy technique in 2 groups of 10 adults Lewis rats using nonionic contrast medium mixed with methylene blue. Each rat had a contralateral vasectomy. A complete vasogram was confirmed by visualization of colored dye in the bladder. An additional group of 5 animals with unilateral vasectomy alone served as controls. The adverse effects of these 2 techniques were assessed by performing mating studies at 2 and 4 months after vasography. In vitro flow through the vas deferens, sperm granuloma formation and histology of the vas deferens at the vasography site were evaluated at sacrifice 5 months after vasography. RESULTS: The fertility of the 3 groups, as measured by the mean number of uterine implantation sites, was not significantly different at the 2 and 4-month breeding periods. In addition, we observed no significant decrease in the fertility of the 3 groups with time. Complete vasal obstruction was noted at sacrifice in 2 rats (20%) in the vasostomy group and none in the puncture or control group (p = 0.476). The mean in vitro flow rates through the vasa of the puncture and vasostomy vasography groups were significantly lower than those in controls (p < 0.05) but not different from each other. The sperm granuloma formation rate was similar among the 3 groups. CONCLUSIONS: Our results demonstrate that both vasography techniques have a measurable adverse effect on vasal flow rates and a potential adverse effect on fertility. The direct puncture method had a slightly lower complication rate than the partial thickness vasostomy method and it may be the preferable technique for the inexperienced microsurgeon.

Animals↗

Dopamine D5 receptor modulates male and female sexual behavior in mice.

RATIONALE: Dopamine exerts its actions through at least five receptor (DAR) isoforms. In female rats, D5 DAR may be involved in expression of sexual behavior. We used a D5 knockout (D5KO) mouse to assess the role of D5 DAR in mouse sexual behavior. Both sexes of D5KO mice are fertile and exhibit only minor disruptions in exploratory locomotion, startle, and prepulse inhibition responses. OBJECTIVE: This study was conducted to characterize the sexual behavior of male and female D5KO mice relative to their WT littermates. METHODS: Female WT and D5KO littermates were ovariectomized and given a series of sexual behavior tests after treatment with estradiol benzoate (EB) and progesterone (P). Once sexual performance was optimal the dopamine agonist, apomorphine (APO), was substituted for P. Male mice were observed in pair- and trio- sexual behavior tests. To assess whether the D5 DAR is involved in rewarding aspects of sexual behavior, WT and D5KO male mice were tested for conditioned place preference. RESULTS: Both WT and D5KO females can display receptivity after treatment with EB and P, but APO was only able to facilitate receptivity in EB-primed WT, not in D5KO, mice. Male D5KO mice display normal masculine sexual behavior in mating tests. In conditioned preference tests, WT males formed a conditioned preference for context associated with either intromissions alone or ejaculation as the unconditioned stimulus. In contrast, D5KO males only showed a place preference when ejaculation was paired with the context. CONCLUSIONS: In females, the D5 DAR is essential for the actions of dopamine on receptivity. In males, D5 DAR influences rewarding aspects of intromissions. Taken together, the work suggests that the D5 receptor mediates dopamine's action on sexual behavior in both sexes, perhaps via a reward pathway.

Animals↗

Interaction between natural and sexual selection during the evolution of mate recognition.

The interaction between natural and sexual selection is central to many theories of how mate choice and reproductive isolation evolve, but their joint effect on the evolution of mate recognition has not, to my knowledge, been investigated in an evolutionary experiment. Natural and sexual selection were manipulated in interspecific hybrid populations of Drosophila to determine their effects on the evolution of a mate recognition system comprised of cuticular hydrocarbons (CHCs). The effect of natural selection in isolation indicated that CHCs were costly for males and females to produce. The effect of sexual selection in isolation indicated that females preferred males with a particular CHC composition. However, the interaction between natural and sexual selection had a greater effect on the evolution of the mate recognition system than either process in isolation. When natural and sexual selection were permitted to operate in combination, male CHCs became exaggerated to a greater extent than in the presence of sexual selection alone, and female CHCs evolved against the direction of natural selection. This experiment demonstrated that the interaction between natural and sexual selection is critical in determining the direction and magnitude of the evolutionary response of the mate recognition system.

Animals↗

A two-locus model of speciation.

Speciation is considered as the evolution of partial or complete cross-incompatibility between the carriers of genes (at a locus called "object locus") that distinguish the prospective species populations. The mating relations at the object locus are modified by the alleles at a second mating modifier locus. Based on a widely applicable concept of fitness and mating preference, it is shown that heterozygote disadvantage in fitness at the object locus is necessary for speciation, which corroborates Wallace's hypothesis. It is pointed out that the difference between sympatric and parapatric speciation essentially lies in the mechanisms stabilizing the polymorphism required at the object locus as a prerequisite for speciation. In the presence of recombination between the object and mating modifier locus speciation may be prevented by forces maintaining gametic phase imbalance between these loci such as can result from unidirectional gene flow between parapatric populations.

Adaptation, Physiological↗

Ethological concepts revisited: immediate early gene induction in response to sexual stimuli in birds.

Courtship behaviors were interpreted by ethologists as being examples of 'sign stimuli' that would act as 'releasers' of stereotypic species-typical behaviors in conspecifics. A key component of the sign stimulus concept is that some form of stimulus filtering occurs that is responsible for the marked selective behavioral responsiveness. Studies of immediate early gene induction in the avian brain in response to conspecific stimuli associated with courtship and mating reveal that such gene induction is highly selective. In male Japanese quail (Coturnix japonica), studies of the immediate early gene c-fos or zenk have been conducted in birds engaging in both appetitive and consummatory aspects of male sexual behavior. High induction of immediate early genes occurs in hypothalamic and limbic areas such as the medial preoptic nucleus, bed nucleus striae terminalis and parts of the archistriatum in birds who had copulated and/or who had expressed a learned social proximity response, reflecting appetitive sexual behavior. Immediate early gene expression was also increased in telencephalic areas such as the hyperstriatum ventrale that presumably plays a role in the integration of sensory cues related to female recognition. In European starlings, studies of zenk induction have been conducted in females who hear male-typical courtship song. Clayton and Mello had shown that zenk is induced in the auditory telencephalon of canaries and zebra finches at high levels specifically in response to conspecific song. Immediate early genes such as fos and zenk are also expressed in song control nuclei specifically in association with song production. In starlings it was found that song was effective in rapidly inducing zenk expression in the auditory telencephalon in males and in females in the breeding as well as in the non-breeding season. Thus, the expression is not greater in females who use song to choose mates or during the breeding season when females are choosing mates. However, there is evidence that high levels of induction in certain areas of the auditory telencephalon in females are greater in response to songs organized in longer bouts that females prefer. Though immediate early gene induction in the brain does not exactly mimic selective behavioral responses to sign stimuli it may represent one important way in which stimulus selectivity of the sort hypothesized previously by Tinbergen and Lorenz is coded. Engaging in species-typical behaviors is also associated with motor-driven immediate early gene expression.

Animals↗

Mate switching as a function of mate quality in convict cichlids, Cichlasoma nigrofasciatum.

We examined mate switching between mated pairs of monogamous convict cichlids as a function of mate quality (size). A mated pair was established in each half of a 284-litre aquarium, an opaque partition separating the two pairs. When the partition was removed, mis-assorted pairs (large males with small females competing with small males with large females) re-sorted themselves such that the larger male and the larger female paired with each other 46% of the time. In contrast, when we exposed initially assorted pairs to each other, large pairs remained intact most of the time and dominated smaller pairs. The pair containing the large male, whether re-sorted or intact, dominated over the other pair and was the only one seen to spawn. Re-sortment resulted both from a preference of males for larger females and of females for larger males, and from the ability of larger individuals to displace their smaller consexual. Small females, however, when paired with a large male, often dominated large females and prevented the large female from mating with the large male. Re-sortment was also influenced by the compatibility of large individuals in their initial pairing situation. Large individuals that had been more compatible with their initial mates were less likely to switch mates. Our results support both the better-option and the incompatibility hypotheses of mate-switching. The availability of more than one breeding site in the aquarium had no effect on the frequency of re-sortment. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.

Journal Article↗

Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid cotesia marginiventris: is quality or quantity important?

Herbivore-induced plant volatiles can function as indirect defense signals that attract natural enemies of herbivores. Several parasitoids are known to exploit these plant-provided cues to locate their hosts. One such parasitoid is the generalist Cotesia marginiventris, which is, among others, attracted to maize volatiles induced by caterpillar damage. Maize plants can be induced to produce the same blend of attractive volatiles by treating them with regurgitant of Spodoptera species. We collected and analyzed the regurgitant-induced emissions of two plant species (cowpea and maize) and of eight Mexican maize varieties and found significant differences among their volatile emissions, both in terms of total quantity and the quality of the blends. In a Y-tube olfactometer. the odors of the same artificially induced plant species and Mexican varieties were offered in dual choice experiments to naive mated females of C. marginiventris. Wasps preferred cowpea over maize odor and, in 3 of 12 combinations with the maize varieties, they showed a preference for the odors of one of the varieties, A comparison of the odor collection with results from the behavioral assays indicates that not only the quantity of the volatile emissions, but also the quality (composition) of the volatile blends is important for attraction of C. marginiventris. The results are discussed in the context of the possibility of breeding crop varieties that are particularly attractive to parasitoids.

Animals↗

Mate recognition in a freshwater fish: geographical distance, genetic differentiation, and variation in female preference for local over foreign males.

It often is assumed that more distant allopatry should reflect reduced rates of contemporary gene flow and/or greater divergence in mate recognition systems. This assumption, however, is rarely tested and may not always be appropriate. Here we investigated female preference for local and foreign males in a morphologically variable Australian freshwater fish, the Pacific blue-eye Pseudomugil signifer. Using a multidisciplinary approach that combined molecular phylogeography with conventional mate choice experiments, we found female blue-eyes spent more time in association with local males only when the alternative was a foreigner from a geographically and genetically more distant population. When offered the choice between two foreign males, females associated more with males from the population that was more closely adjacent to their own. Our results suggest that female preference for local over foreign males in blue-eyes may depend on how genetically and geographically separated populations are from one another.

Animals↗

Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change.

UV vision has profound effects on the evolution of organisms by affecting such behaviors as mating preference and foraging strategies. Despite its importance, the molecular basis of UV vision is not known. Here, we have transformed the zebra finch UV pigment into a violet pigment by incorporating one amino acid change, C84S. By incorporating the reverse mutations, we have also constructed UV pigments from the orthologous violet pigments of the pigeon and chicken. These results and comparative amino acid sequence analyses of the pigments in vertebrates demonstrate that many avian species have achieved their UV vision by S84C.

Amino Acid Sequence↗

Population density influences male-male competition in guppies.

This study tested the general prediction that population density affects male-male competition, female mate choice and the opportunity for sexual selection. By manipulating the density of guppies, Poecilia reticulata, while keeping the sex ratio constant, I found that male mating tactics were phenotypically plastic with respect to density. As density increased, males decreased their courtship displays. Male-male competition and mate searching were highest at intermediate densities. Population density had no significant effect on the total number of copulations, copulatory tactics or the percentage of postcopulatory guarding. Female preference for males with a higher percentage of orange coloration was similar at all density levels. The 'opportunity for sexual selection', which estimates the upper limit to which a selected trait can shift if directional selection is operating and was calculated as the variance in number of copulations per male divided by the square of the mean number of copulations, was negatively associated with population density. This may be due to the decrease in male-male competition at high density rather than female preference which was similar across density treatments. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

Males call more from wetter nests: effects of substrate water potential on reproductive behaviours of terrestrial toadlets.

Laboratory studies of terrestrial-breeding frogs have demonstrated that wetter substrates produce fitter offspring but the relevance of substrate wetness to adult reproductive strategies is unknown. I hypothesized that male toadlets (Pseudophryne bibronii) would select wetter areas for nesting and would advertise wet nests strongly, and tested these predictions by manipulating water potentials at a breeding site. Males preferred to nest in the wettest areas, and called at greater rates on almost twice as many nights as males occupying drier nests. Overall, males that mated called on significantly more nights than unmated males. Hence, because males occupying wet nests called more, they also mated more and in 19 out of 20 cases, oviposition occurred in wet nests that were suitable for embryonic development. Males occupying drier nests may have risked dehydration by calling, and so were less able to signal to females. Hydration states therefore have the potential to influence the reproductive success of terrestrial male frogs.

Animals↗