Reversal of mating preference by crossing strains of Drosophila melanogaster.
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Here we use sexual selection theory to develop a logistically simple, yet effective, method for the manipulation of female reproductive behavior for conservation goals. Mate choice leading to nonrandom mating patterns can exacerbate the loss of genetic diversity in small populations. On theoretical grounds, females should choose high-quality mates. A prediction stemming from chemical communication theory is that competitive males will be better able to saturate an area with scent marks. If this is true, females should mate preferentially with males whose odors they encounter most frequently. We tested this hypothesis with the pygmy loris, Nycticebus pygmaeus, a threatened and poorly studied nocturnal prosimian. For several weeks females were exposed repeatedly to the urine from a particular male, and were then allowed to choose between a male whose odors were familiar and one whose odors were novel. Females showed an unusually strong preference for the familiar-odor male, as indicated by several behavioral measures of mate preference. Conservation managers can use this method as a tool to obtain reproductive pairings that will maximize genetic compatibility and diversity. For example, unsuccessful males may be given the opportunity to reproduce. In captive populations, studbook managers often select pairs in order to optimize outbreeding, but these selected pairings may not coincide with the preferences of the individual animals involved. Although several authors have made theoretical arguments for manipulating mate choice for conservation, this is a novel test of a proximate mechanism that can be manipulated, cultivating applications rather than mere implications.
We examined the effects of odor exposure in the nest on the offspring's subsequent adult responsivity to pups scented with the same odor or a different odor. It was hypothesized that animals receiving exposure to the odor in the nest would be more maternally responsive to pups scented with the (same) exposed odor than to unscented (water-scented) pups. In the first part of the study (Part A), Sprague-Dawley female rat pups (days 1-18 of age) either received exposure to an artificial lemon odor or to the natural (water) odor in the nest. In the second part of the study (Part B), rat pups were exposed daily to lemon or neutral odorants in an incubator at a distance from the mother and the nest. On day 21, animals received odor preference tests for lemon versus neutral pine bedding. On day 60, animals were mated and their pups were removed at 15-min intervals at the time of parturition. Animals were then tested for maternal behavior to foster pups on day 1 or 7 after parturition. Foster pups were scented either with the lemon odor or with water (unscented). Early exposure to lemon in the nest context enhanced animals' attraction to the lemon odor in juvenile tests. In adult maternal tests, exposure to odor on the mother and in the nest had two effects. It increased the latency for animals to express maternal behavior; however, once mothers expressed maternal behavior, they spent more time licking and crouching over pups scented with the same odorant to which they had been exposed earlier on their own mothers. Simple exposure to the lemon odorant out of context of the nest had no effect on adult maternal latencies or behavior.
Female and male animals often choose mates based upon the complementarity of their courtship behaviours and preferences. The importance of this fact on the evolutionary dynamics of populations has long been appreciated. What has not been appreciated is the role that social learning might play in the transmission of systems of courtship behaviour across generations. This paper addresses the social transmission of courtship behavioural traditions in vertebrates. It discusses views of culture in the context of behavioural signals and preferences in courtship. It then reviews empirical evidence for culture-like processes affecting courtship behaviour, focusing on studies of song learning in passerine birds and work on social learning of mating preferences. The paper concludes with potential future directions for research on social traditions in systems of courtship behaviour, including determining mechanisms of transmission, genetic and non-social environmental effects, and selective factors influencing the stability of behavioural traditions over time. By integrating proximate and ultimate questions for the transmission of courtship systems, this work would increase our understanding of the ways individual development, cultural processes, and population evolution influence, and are in turn influenced by, one another.
Genetic heterozygosity is thought to enhance resistance of hosts to infectious diseases, but few tests of this idea exist. In particular, heterozygosity at the MHC, the highly polymorphic loci that control immunological recognition of pathogens, is suspected to confer a selective advantage by enhancing resistance to infectious diseases (the "heterozygote advantage" hypothesis). To test this hypothesis, we released mice into large population enclosures and challenged them with multiple strains of Salmonella and one of Listeria. We found that during Salmonella infections with three avirulent strains, MHC heterozygotes had greater survival and weight than homozygotes (unlike sham controls), and they were more likely to clear chronic Salmonella infection than homozygotes. In laboratory experiments, we found that MHC heterozygosity enhanced the clearance of multiple-strain Salmonella infections. Yet, contrary to what is widely assumed, the benefits of heterozygosity were due to resistance being dominant rather than overdominant, i.e., heterozygotes were more resistant than the average of parental homozygotes, but they were not more resistant than both. The fact that MHC heterozygotes were more resistant to infection and had higher fitness than homozygotes provides a functional explanation for MHC-disassortative mating preferences.
A critical prediction of the immunocompetence handicap hypothesis is that the expression of secondary sexual traits should be positively correlated with pathogen resistance ability This correlation is necessary if females are to be able to use a particular sexual trait as an indicator of a male's resistance ability. In this study we document a positive correlation between a sexually selected component of the calling song of male house crickets (the number of syllables per chirp) and haemocyte load, an important determinant of the ability to encapsulate pathogens in insects. The results indicate that, by favouring males which produce more syllables per chirp, females may also select males with higher pathogen resistance ability, potentially generating either direct or indirect selection on female mating preferences.
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A partner preference paradigm, stud male vs estrous female, was used to study sexual behavior. Ovariectomized Wistar rats received bilateral electrolytic (n = 33) or sham (n = 16) lesion of the nucleus accumbens. Animals were tested in two different experimental situations, either with stimulus animals tethered (test with possibility of mating) or with stimulus animals behind a wire mesh (test without possibility of mating). Each test was carried out once prior to surgery and twice postoperatively following priming with estradiol benzoate and progesterone. Lordosis, rejection behaviors and soliciting patterns were scored in tests with tethered stimulus animals. The tendency of the experimental female to approach and remain in the vicinity of each stimulus animal was quantified to study the partner preference. Nucleus accumbens lesion increased the number of rejection responses to male mount attempts without modifying either receptivity estimated by lordosis reflex or soliciting behaviors. Control females showed a statistically significant preference for the male throughout the experiments. Lesioned females exhibit a preference for the male only in the test without sexual interaction possibility. This preference disappeared in the test with possibility of mating and it was even reversed when the male showed copulatory activity. These results, together with the absence of changes in lordosis behavior and soliciting activity, suggest that both the inversion in preference and the higher levels of mount rejections found in the lesioned animals are more likely attributable to hyperreactivity to the copulatory stimulus rather than an alteration in the female's rat sexual motivation.
Mating activity was observed during four breeding seasons in two groups of black and white ruffed lemurs (Varecia variegata variegata) living in lowland rain forest on Nosy Mangabe island, Madagascar. The onset of the May-July breeding season was signalled by behavioral changes in adult males. Males made forays outside their usual home ranges, were more aggressive to other males, and performed appetitive and other sex-specific behaviors more frequently. Females showed receptive and proceptive behaviors during a 1-2 day behavioral estrus. Ruffed lemurs mated monogamously, polyandrously, and polygynously. These observations do not support previous assertions that they live only in monogamous families. Limited evidence suggests females exercised mate choice and may have preferred familiar males.
Filial cannibalism (the consumption of one's own viable offspring) is common among fish with paternal care. In this study, I use a computer simulation to study simultaneous evolution of male filial cannibalism and female mate choice. Under certain conditions, selection on parental males favors filial cannibalism. When filial cannibalism increases a male's probability to raise the current brood successfully, filial cannibalism also benefits the female. However, when egg eating is a male investment into future reproduction, a conflict between female and male interests emerges. Here I investigate how female discrimination against filial cannibals affects evolution of filial cannibalism and how different female choice criteria perform against filial cannibalism. The introduction of discriminating females makes the fixation of filial cannibalism less likely. I introduced three different female choice criteria: (1) females who could discern a male's genotype, that is, whether the male was going to eat eggs as an investment in future reproductive events; (2) energy-choosing females that preferred to mate with males who had enough energy reserves to live through the current brood cycle without consuming eggs; and (3) females that preferred to mate with already mated males, that is, males with eggs in their nest. Genotype choice never coexisted with filial cannibals at fixation and filial cannibals were unable to invade a population with genotype-choosing females. Energy choice was successful only when males had high energy reserves and were less dependent on filial cannibalism as an alternative energy source. The egg choosers frequently coexisted with the cannibals at fixation. When the female strategies were entered simultaneously, the most frequent outcome for low mate sampling costs was that both the cannibals and the egg choice was fixed and all other strategies went extinct. These results suggest that sexual conflicts may not always evolve toward a resolution of the conflict, but sometimes the stable state retains the conflict. In the present case, this was because the egg-preference strategy had a higher fitness than the other female strategies. The outcome of this simulation is similar to empirical findings. In fish with paternal care, male filial cannibalism and female preference for mates with eggs commonly co-occur.
Minority male mating advantage was tested in wild type strains of Drosophila ananassae through multiple-choice experiments. Mating success of two types of flies present in five different ratios was scored by direct observation in an Elens-Wattiaux mating chamber. We found no evidence for minority male mating advantage in wild type strains of D. ananassae. The relative mating success of two types of females was also compared in the multiple-choice experiments at different ratios; there was no evidence for a rare female effect. Further, there was similarity in the results of experiments employing different methods. The total number of homogamic and heterogamic matings was obtained by combining the data (all five ratios) from each experiment. Homogamic matings were significantly more frequent than heterogamic ones, which demonstrates preferential mating between males and females of the same strain; this was also supported by a lower isolation estimate. There was also a significant difference in the degree of mating preference between the two strains.
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A quantitative genetic model of the joint evolution of female mating preferences and sexual dimorphism in homologous characters of the sexes is described for polygamous species with no male parental effort, such that mating preferences are selectively neutral and evolve only by indirect selection on genetically correlated characters. The male character and the homologous female character are each under stabilizing natural selection toward an optimum phenotype. At an evolutionary equilibrium the female character under natural selection is at its optimum, whereas there is a line of possible equilibria between female mating preferences and the male character. The line of equilibria may be stable or unstable, depending on the intensity of natural selection, the type of mating preferences, and the inheritance of the characters. Various mechanisms for maladaptive evolution of mating preferences and sexual dimorphism are discussed.
Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.
Many animals obtain reliable information about potential mates, including whether they are parasitised or not, mostly from olfactory cues in urine. Previous experiments with rodents have shown that females can detect parasites in males that are potentially transmissible during copulation, so that females can directly avoid infection by discriminating against parasitised males. Here, using choice tests, we examine whether female rats can distinguish males infected with the tapeworm Hymenolepis diminuta Rudolphi, 1819, a parasite with a complex life cycle and thus not directly transmissible among rats. Female rats tended to spend more time investigating the urine of non-parasitised males than that of parasitised males. The magnitude of the parasite burden in the infected males had no effect on the females' preference for the non-parasitised males. We also found that parasitised males had lover testosterone levels in their blood than non-parasitised males. These results suggest that females use cues in male urine reflecting either the presence of the parasite and/or lower testosterone levels to avoid parasitised males and possibly secure resistance genes for their offspring.
REVIEW Recent approaches to analyzing the evolution of female mating preferences emphasize how historical influences on female receiver systems can bias the evolution of male traits that females find attractive. These studies combine animal behavior, sensory biology, phylogenetics, and artificial neural network models. They attempt to understand why specific phenotypes involved in sexual selection have evolved, rather than merely determining whether such traits and preferences are adaptive. It is now clear that traits and preferences often do not coevolve via genetic correlations, that female mating preferences for a given male trait are influenced by adaptations and constraints outside of the context of female responses to that particular trait, and that receiver biases can explain much of the diversity in male signaling phenotypes. It also appears that an understanding of historical effects will prove valuable in investigating why neural and cognitive systems respond to sensory stimuli as they do.