The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.     

Repeatability of Male Mate Choice in the Mosquitofish, Gambusia holbrooki

Male mate choice has evolved in many species in which female fecundity increases with body size. In these species, males are thought to have been selected to favour mating with large females over smaller ones, thereby potentially increasing their reproductive success. While male mate choice is known to occur, it is less well studied than female mate choice and little is known about variation in mating preference among individual males. Here, we presented individual male eastern mosquitofish ( Gambusia holbrooki ) with paired females that differed in body size, and we quantified their mate preference on two consecutive days, allowing us to assess repeatability of preferences expressed. When males were allowed to view paired stimulus females, but not to acquire chemical or tactile cues from them, they exhibited a strong preference for large females over smaller ones. However, individual males were not consistent in the strength of their preference and repeatability was not significant. When individual males were allowed to fully interact with pairs of females, the males again exhibited a preference for large females over smaller ones, as revealed by a greater number of attempted copulations with large females than with smaller ones. In the latter social context, individual male preference was significantly repeatable. These results indicate that male eastern mosquitofish from our Florida study population possess, on average, a mating preference for larger females and that this preference is repeatable when males socially interact freely with females. The significant repeatability for mating preference, based on female body size, obtained for male mosquitofish in the current study is consistent with the presence of additive genetic variation for such preferences in our study population and thus with the opportunity for the further evolution of large body size in female mosquitofish through male mate choice.     

Male mate choice in a sexually cannibalistic species: male escapes from hungry females in the praying mantid <Emphasis Type="Italic">Tenodera angustipennis</Emphasis>

While competing males and choosy females may be common in animal mating systems, male choice can evolve under certain conditions. Sexual cannibalism is such a condition because of the high mortality risk for males. In mantids, female body condition is associated with male mate preference, with fat females preferred, due to at least two reasons: females in poor nutritional condition are likely to attack and predate males, and fat females can potentially increase the number of offspring. Thus, the risk of cannibalism and female fecundity can influence male mating behavior. In this study, we attempted to separate these factors by using the praying mantid Tenodera angustipennis to examine whether male preference for fat female mantids was based on avoiding sexual cannibalism (cannibalism avoidance hypothesis) or preference for female fecundity (fecundity preference hypothesis). The feeding regimes were experimentally manipulated to discriminate between the effects of female fecundity and female hunger status on male and female mating behaviors. We found that recently starved females more frequently locomoted toward the male, and that male abdominal bending was less intensive and escape was sooner from recently starved females. These female and male behavioral responses to female hunger condition may reveal male avoidance of dangerous females in this mantid.     

Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice

Parasites can affect mate choice, with females preferentially selecting parasite-free males. Prior exposure to, or experience with, males has also been suggested to influence mate responses. Here, we examined the effects of an immediate, brief (1 or 15 min) pre-exposure to the urinary and associated odours of either an uninfected male house mouse,Mus domesticus , or a male infected with the natural murine nematode parasite, Heligomosomoides polygyrus, on the subsequent responses of female mice to the odours of infected and uninfected males. Using an odour preference test we found that females displayed a marked overall preference for the odours of uninfected males. Pre-exposure to the odours of a parasitized male decreased female preference for nonparasitized males and increased female preference for parasitized males. This ‘prior male’ effect was evident for both the total odour preference and initial odour choice. Females pre-exposed to the odour of a parasitized male displayed decreased choosiness and made no particular initial choice of a male, while still maintaining an overall preference for the odours of uninfected males. These shifts in initial choice and odour preference were not directly associated with either female stress responses or stress-related odour cues of the males. Our findings show that female mice can distinguish between parasitized and nonparasitized males on the basis of odour and suggest that a brief exposure to the odours of infected males influences females' immediate odour preferences, and their subsequent preference for and choice of males. This rapid, infection-associated ‘prior male’ effect may contribute to the reported variations in female mate preference and choice. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

The Effect of Female Quality on Male Ejaculatory Expenditure and Reproductive Success in a Praying Mantid

Strategic ejaculation is a behavioural strategy shown by many animals as a response to sperm competition and/or as a potential mechanism of cryptic male choice. Males invest more mating resources when the risk of sperm competition increases or they invest more in high quality females to maximize their reproductive output. We tested this hypothesis in the false garden mantid Pseudomantis albofimbriata, where females are capable of multiply mating and body condition is an indicator of potential reproductive fitness. We predicted male mantids would ejaculate strategically by allocating more sperm to high quality females. To determine if and how males alter their ejaculate in response to mate quality, we manipulated female food quantity so that females were either in good condition with many eggs (i.e. high quality) or poor condition with few eggs (i.e. low quality). Half of the females from each treatment were used in mating trials in which transferred sperm was counted before fertilisation occurred and the other half of females were used in mating trials where fertilisation occurred and ootheca mass and total eggs in the ootheca were recorded. Opposed to our predictions, the total number of sperm and the proportion of viable sperm transferred did not vary significantly between female treatments. Male reproductive success was entirely dependent on female quality/fecundity, rather than on the number of sperm transferred. These results suggest that female quality is not a major factor influencing postcopulatory male mating strategies in P. albofimbriata, and that sperm number has little effect on male reproductive success in a single mating scenario.     

Does sexual experience affect the strength of male mate choice for high‐quality females in Drosophila melanogaster?

Although females are traditionally thought of as the choosy sex, there is increasing evidence in many species that males will preferentially court or mate with certain females over others when given a choice. In the fruit fly, Drosophila melanogaster, males discriminate between potential mating partners based on a number of female traits, including species, mating history, age, and condition. Interestingly, many of these male preferences are affected by the male''s previous sexual experiences, such that males increase courtship toward types of females that they have previously mated with and decrease courtship toward types of females that have previously rejected them. D. melanogaster males also show courtship and mating preferences for larger females over smaller females, likely because larger females have higher fecundity. It is unknown, however, whether this preference shows behavioral plasticity based on the male''s sexual history as we see for other male preferences. Here, we manipulate the sexual experience of D. melanogaster males and test whether this manipulation has any effect on the strength of male mate choice for large females. We find that sexually inexperienced males have a robust courtship preference for large females that is unaffected by previous experience mating with, or being rejected by, females of differing sizes. Given that female body size is one of the most common targets of male mate choice across insect species, our experiments with D. melanogaster may provide insight into how these preferences develop and evolve.     

Alternative reproductive tactics in male freshwater fish influence the accuracy of species recognition

Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice‐associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

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.     

INTERSEXUAL SELECTION IN THE MEDITERRANEAN FRUIT FLY: DOES FEMALE CHOICE ENHANCE FITNESS?

Adaptive hypotheses of female choice predict that females use male courtship displays as an indicator of male quality. A test of whether female choice is adaptive measuring direct and indirect effects of mate choice on females was made using a laboratory population of a lek-mating species, the Mediterranean fruit fly. The nonrandom mating observed in this species is thought to be strongly influenced by female choice. Whether female choice acts to increase fecundity or offspring quality was assessed using two different statistical tests. Multiple regression showed that females generally do not receive direct benefits as a result of mating with males which are successful in copulating with many females. However, in one trial the relationship between male quality and female benefit was nonlinear. Females which mate with males that obtain few matings (<2), and females which mate with males that obtain many matings (>6) enjoy increased fecundity. Mate choice does not, however, appear to enhance offspring quality as father/son correlation and sibling analysis showed no heritable component to male copulatory success.     

Mate guarding and male mate choice in the chameleon grasshopper <Emphasis Type="Italic">Kosciuscola tristis</Emphasis> (Orthoptera: Acrididae)

In the wild, male chameleon grasshoppers (Kosciuscola tristis) are frequently observed mounted on the back of females even when not in copula, and will fight off other usurping males. If this behaviour is mate guarding and reflects investment in male mate choice, then we expect males to preferably guard females based on reliable cues of quality. Cues for female quality likely include female size and egg development that together may indicate fecundity. We investigated male mate choice in the field expressed as mate-guarding preference, by comparing size and egg development in guarded and unguarded females. We found no difference between guarded and unguarded females in measures of fecundity or body size. The majority of females sampled did not contain any viable eggs. This finding suggests that male K. tristis indiscriminately guard females in a scramble mating system.     

Female mate choice is not affected by mate condition in a fish with male care

Several studies have shown that mate choice based on condition leads to higher reproductive success of the choosing individual. Yet, a growing body of literature has failed to find support for mate choice based on mate condition, even when the choosing individual would clearly benefit from such a choice. This indicates that animals’ mate choice is often more complex than currently appreciated and that even well-founded expected preferences cannot be taken for granted. Using the broad-nosed pipefish, Syngnathus typhle, we manipulated male condition experimentally to explore whether it affects female mate choice. In this sex-role-reversed species, males care for the offspring in a specialised brood pouch. Males are the choosier sex, but given the opportunity, females are selective as well. During brooding, males can both provide embryos with nutrients and take up nutrients that originate from eggs deposited in the pouch, and embryo survival correlates positively with male condition. Together, this suggests that it would be beneficial for females to mate with males in high condition. However, we found no female preference for males in better condition. Thus, this study adds to the literature of mate choice that is unaffected by mate condition. Possible reasons for our result are discussed.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.     

Context‐ and State‐Dependent Male Mate Choice in a Sexually Cannibalistic Spider

High male mating investment may favor selection on male mate choice particularly if females vary in quality. Terminal investment strategies constitute a maximal mating effort and have evolved independently in the absence of paternal investment in several spider taxa including the genus Argiope. To test for male mate preferences in the above context, we used the sexually cannibalistic spider A. bruennichi. We varied male state (mating status and post‐maturation age) as well as the competitive context and quantified male mate choice decisions between females of different states and developmental stages in binary choice tests. We found an overall adaptive preference for the virgin against the mated female regardless of male mating state. Furthermore, we demonstrated that older males paid more attention to female fecundity‐related traits than to mating status. In a second set of experiments, we offered males a choice between a virgin and a subadult female and varied the competitive context which had no effect on male decisions. Curiously, a preference for the virgin adult female was only apparent after exclusion of females that matured <3 d prior to the test. Repeated tests of males supported the hypothesis that males do not distinguish between a freshly matured virgin female and a subadult female. Our results show that male spiders execute mate choice based on information collected from female silk strands and that they integrate their own state into mating decisions.     

A cost of Wolbachia-induced sex reversal and female-biased sex ratios: decrease in female fertility after sperm depletion in a terrestrial isopod

A number of parasites are vertically transmitted to new host generations via female eggs. In such cases, host reproduction is an intimate component of parasite fitness and no cost of the infection on host reproduction is expected to evolve. A number of these parasites distort host sex ratios towards females, thereby increasing either parasite fitness or the proportion of the host that transmit the parasite. In terrestrial isopods (woodlice), Wolbachia bacteria are responsible for sex reversion and female-biased sex ratios, changing genetic males into functional neo-females. Although sex ratio distortion is a powerful means for parasites to increase in frequency in host populations, it also has potential consequences on host biology, which may, in turn, have consequences for parasite prevalence. We used the woodlouse Armadillidium vulgare to test whether the interaction between Wolbachia infection and the resulting excess of females would limit female fertility through the reduction in sperm number that they receive from males. We showed that multiple male mating induces sperm depletion, and that this sperm depletion affects fertility only in infected females. This decrease in fertility, associated with male mate choice, may limit the spread of Wolbachia infections in host populations.     

Diet affects female mating behaviour in a seed‐feeding beetle

In species where males provide nuptial gifts, females can improve their nutritional status and thus increase their fecundity by mating when in need of resources. However, mating can be costly, so females should only mate to acquire resources when the need for resources is large, such as when females are nutritionally‐deprived. Two populations of the seed‐feeding beetle Callosobruchus maculatus, a species that produces relatively large nuptial gifts, are used to test whether female nutritional status affects mating behaviour. Female access to water, sugar and yeast are manipulated and the fitness consequences of these manipulations are examined together with the effects of diet on the propensity of nonvirgin females to mate. Access to water has a small but significant effect on mass loss over time, lifespan and fecundity of females, relative to unfed controls. Access to sugar (dissolved in water) improves female fecundity and lifespan above that of hydrated females but access to yeast has no positive effects on female survival or reproduction. Diet has a large effect on both receptivity of nonvirgin females to a male and how quickly they accept that male. Unfed females are both more likely to mate, and accept a mate more quickly, than females provided access to water, which are more likely to mate and accept a mate more quickly than females provided with sugar. This rank order of behaviours matches the order predicted if females increase their mating rate when nutritionally deprived (i.e. it matches the effect of diet on female fitness). The results obtained also suggest that mate choice may be condition‐dependent: females from one population (Burkina Faso) show a preference for large males when well‐fed but not when unfed, although this result is not found in a second population (South India). It is concluded that nutritionally‐deprived females are more receptive to mates than are well‐fed females, consistent with the hypothesis that females ‘forage’ for nuptial gifts, or at least more willingly accept sperm in exchange for nuptial gifts, when they are nutritionally deprived.     

Male and Female Mating Behavior is Dependent on Social Context in the Butterfly Bicyclus anynana

Reproduction is often more costly to females than it is to males, leading to the evolution of ornamented or competitive males and choosy females. Reproduction costs to females, however, can be reduced through nuptial gifts provided by males. These gifts, by increasing female survival or fecundity, can promote the evolution of mutual mate choice, ornamentation, or competition in both sexes, as well as plasticity in mating behavior dependent on social context. We tested for plasticity in male and female mating behavior in a species of butterfly, Bicyclus anynana, where male spermatophore gifts contribute to female survival and fecundity, and where mutual mate choice and ornamentation were previously established. We examined the effect of a sexual competitor on male–female interactions by observing and comparing the behavior of male–female pairs with that of triads containing either an extra male or an extra female. In the presence of a sexual competitor both males and females copulated less than when in male–female pairs, regardless of the direction of sex-ratio skew. Active males increased their own likelihood to copulate, while active females increased their likelihood of being courted. In addition, there was an effect of social context on relative rates of male and female courting and flying. These results suggest that both males and females change their mating behavior in response to social context in the butterfly Bicyclus anynana.     

Do males choose their mates in the lekking moth Achroia grisella? Influence of female body mass and male reproductive status on male mate choice

Lekking males aggregate to attract females and contribute solely to egg fertilization, without any further parental care. Evolutionary theory therefore predicts them to be nonchoosy toward their mates, because any lost mating opportunities would outweigh the benefits associated with such preferences. Nevertheless, due to time costs, the production of energetically costly sexual displays, and potential sperm limitation, the mating effort of lekking males is often considerable. These factors, combined with the fact that many females of varying quality are likely to visit leks, could favor the evolution of male mate preferences. Here, we show that males of the lekking lesser wax moth, Achroia grisella, were indeed more likely to mate with heavier females in choice experiments, even at their virgin mating (i.e., when their reproductive resources have not yet been depleted by previous matings). This differential female mating success could not be attributed to female behavior as heavy and light females showed similar motivation to mate (i.e., latency to approach the males) and time to copulate. Males seem to benefit from mating with heavier females, as fecundity positively correlated with female mass. This new empirical evidence shows that male mate choice may have been underestimated in lekking species.     

Aversive Responses of Female Mice to the Odors of Parasitized Males: Neuromodulatory Mechanisms and Implications for Mate Choice

The detection and avoidance of parasitized conspecifics is proposed to have important consequences for the behavior of animals, especially as related to mate choice. A reduction in pain sensitivity (i.e. analgesia) is a major correlate of exposure to real or potential danger and threatening stimuli, facilitating the expression of various active (e.g. fleeing) and passive (e.g. immobilization) defense responses. The present study examined pain sensitivity (latency of a foot-lifting response to 50 ° C thermal surface) of female mice, Mus musculus, that were exposed to the urine and other odor secretions of male mice subclinically infected with the naturally occurring, enteric, sporozoan parasite, Eimeria vermiformis. A 30-min exposure to the odors of a parasitized male induced an analgesia in the female mice that was found to be mediated by the increased activity of endogenous opioid peptide systems. A brief 1-min exposure to the male odors induced a shorter duration and lower amplitude analgesia of a non-opioid (serotonergic) nature. Maximum analgesic responses were induced by the odors of pre-infective [5 days post-infection (PI)] and infective (day 10 PI) males, with significantly lower responses elicited by the odors of post-infective (day 17 PI) male mice. Exposure to the odors of unparasitized males had no significant effects on the pain sensitivity of female mice. These results indicate that female mice can distinguish between the odors of parasitized and non-parasitized male mice, and find the odors of parasitized males threatening and/or stressful. These odor-induced analgesic responses and their neurohormonal correlates may be part of an adaptive preparatory defense mechanism that facilitates the detection and avoidance of parasitized males by female mice and contributes to female mate choice.     

Male mate choice in Tibetan macaques Macaca thibetana at Mt. Huangshan, China

Though females are generally more selective in mate choice, males may also benefit from mate choice if male reproductive success is limited by factors other than simply the number of female mates, and if females differ in short-term reproductive potential. We studied male mate choice in a free-ranging troop of Tibetan macaques Macaca thibetana at Mt. Huangshan,China, from August 2007 to April 2008. We employed focal animal sampling and all occurrence sampling to record sexual related behaviors. Eight adult females were divided into three female quality categories according to the females' age, rank and parity.Using male mating effort as a proxy for male mate choice, we found that males do distinguish female quality and show time-variant mating strategies. Specifically, females with dominant rank, high fecundity, and middle age attracted significantly more males. Our results suggest that female short-term reproductive potential appears to be an important variable in determining male mating effort. Male Tibetan macaques do exercise mate choice for higher quality females as well as reduce useless reproductive cost, which is consistent with the direct benefits theory of mate choice.     

Divergent Preferences for Song Structure between a Field Cricket and its Phonotactic Parasitoid

In many animals, males produce signals to attract females for mating. However, eavesdropping parasites may exploit these conspicuous signals to find their hosts. In these instances, the strength and direction of natural and sexual selection substantially influence song evolution. Male variable field crickets, Gryllus lineaticeps, produce chirped songs to attract mates. The eavesdropping parasitoid fly Ormia ochracea uses cricket songs to find its hosts. We tested female preferences for song structure (i.e., chirped song vs. trilled song) in crickets and flies using choice experiments. Female crickets from a parasitized and a non-parasitized population significantly preferred the species-typical chirped song, whereas flies significantly preferred a trilled song, which is expressed by other hosts in different regions. Sexual selection due to female choice and natural selection due to fly predation both appear to favor the chirped song structure of G. lineaticeps in the parasitized population, whereas sexual selection favors the chirped structure in the non-parasitized population.