Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice

There is accumulating evidence that females may preferentially select parasite-free or -resistant males. Minimal attention has, however, been paid to the mate preferences and responses of the parasitized male hosts themselves. Here, we considered the effects of parasitic infection on male host mate responses, the neuromodulatory correlates of these responses, and the relations of these responses to female mate choice. Using an odor “preference” test, we examined the effects of different stages of an acute, sub-clinical infection with the naturally occurring, enteric, single host, protozoan parasite, Eimeria vermiformis, on the responses of male mice, Mus musculus domesticus, to the odors of estrous females along with the responses of uninfected females to the parasitized males. At 4 days post-infection (non-infective, pre-patent stage) E. vermiformis-infected male mice showed a significantly decreased preference for the odors of estrous females, whereas at 10 days post-infection (infective, patent stage) infected males showed a significantly increased preference for the odors of estrous females. Parasitized males displayed no significant changes in their responses to the odors of non-estrous females, supporting effects on the reproductively related responses of the host. In parallel, estrous females displayed a reduced interest in the odors of infected males. Least interest was expressed in the odors of the patent, infective males, consistent with the avoidance of contagion. Using selective opioid peptide receptor agonists and antagonists we found evidence that enhanced kappa opioid peptide (e.g., dynorphin) activity was related to the decreased sexual interest of the pre-infective males, while augmented delta opioid peptide (e.g., enkephalin) activity was associated with the enhanced responses of the infective males to females. We further showed that acute kappa opiate administration reduced the responses of uninfected males to females and that uninfected females displayed modified responses to the odors of uninfected males subject to acute modifications of opioid activity. We suggest that these differential shifts in endogenous opioid activity in the parasitized males are associated with and, or related to alterations in neuro-immune and endocrine functions. These findings show that parasitic infection can have, depending on the stage of infection and associated neuromodulatory changes, either significant facilitatory or inhibitory effects on male host preferences for and responses to females. Received: 22 April 1996 / Accepted after revision: 15 March 1997     

Unattractiveness of mated females to males in the parasitoid wasp Spalangia endius

Despite common stereotypes, males are not always indiscriminate and eager when it comes to mating. In the parasitoid wasp Spalangia endius, the initial response of males to females was almost always one of apparent excitement; however, this was followed by a clear preference for virgin females over mated females in both no-choice and choice situations. The no-choice data were collected from videotapes of male-female pairs of all possible combinations of mated and virgin individuals. Neither female nor male mating status had a significant effect on likelihood of, or time until, contact or male courtship fanning. However, a males first retreat was sooner when the female was mated than when she was virgin; mated males exhibited their first retreat sooner than did virgin males; and mated females were less likely to be mounted than were virgin females. In addition to the videotapes, male-choice experiments were performed. When given a choice of a virgin and a mated female, both virgin and mated males were more likely to mount and copulate with the virgin. The difference in response to virgin versus mated females seemed to be less in virgin males than in mated males, perhaps due to virgin males greater eagerness to mate: when a virgin male and a mated male were presented with a dead virgin female, the virgin male was usually the first to respond to the female. That males preferentially retreated from and avoided mounting mated females appears to be adaptive given that mated females rarely copulated.Communicated by N. Wedell     

Reduced costs of mixed-species pairings in flycatchers: by-product or female strategy?

Heterospecific matings are generally assumed to be unconditionally disadvantageous due to reduced viability or fertility of hybrid offspring. For female collared flycatchers (Ficedula albicollis) mated to male pied flycatchers (Ficedula hypoleuca), the cost of heterospecific pair formation is reduced due to high levels of conspecific extra-pair paternity and a male-biased offspring sex ratio. In order to investigate whether these cost-reducing mechanisms are the result of female mating strategies, rather than being a by-product of species incompatibilities, we manipulated the plumage of male collared flycatchers before pair formation to make them resemble male pied flycatchers. Since species incompatibilities are absent in this design, any systematic effect of manipulation on sex ratio or paternity would indicate a role of female mating strategy. Paternity was determined by means of a likelihood approach that controls the errors made in assigning a chick to be ‘within-pair’ or ‘extra-pair’. Neither the sex ratio nor the male share of paternity was affected by the manipulation in a systematic manner. We therefore conclude that our experimental data provide no support for the suggestion that female behavioural strategies are markedly adjusted in response to formation of mixed-species pairs. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Why is the coral-reef fish Valenciennea strigata (Gobiidae) monogamous?

Parental-investment theory predicts that monogamy should be rare, and empirical evidence supports this prediction. Monogamy has generally been explained by either (1) a need for biparental care, or (2) a uniform distribution of limiting resources. By contrast, monogamy has evolved in several coral-reef fishes without biparental care, and many coral-reef fishes may not be limited by resources. Monogamy in these fishes might be explained by either (3) a low population density that favors mate fidelity, or (4) an abundance of resources that allows all males to breed and thus lowers the cost-benefit ratio for females that mate guard. We tested predictions of these hypotheses in the coral-reef fish, Valenciennea strigata, except that (1) biparental care had previously been rejected. We found no evidence of resource limitation (2a): food densities within territories did not differ from the density of food in unused habitat adjacent to territories; potential nest sites also existed in this unused habitat. Similarly, (2b) if resources limit the population, territory defense might require the coordinated efforts of a pair; however, widowed fish maintained their territories and (3) remated rapidly. Finally, (4) all males maintained a nest, both sexes enforced monogamy by mate guarding, and females benefited from guarding a high-quality (large) mate. Females mated to large males fed more than when they paired with small males. The results support the hypothesis that abundant and uniformly distributed resources can lead to monogamy by lowering the cost of guarding a mate when mate guarding provides benefits. Received: 25 November 1997 / Accepted after revision: 29 December 1997     

Offspring genetic diversity increases fitness of female Atlantic salmon (Salmo salar)

Inbreeding has negative effects on individual and population performances. Therefore, enhancement of offspring genetic diversity is believed to play a major role in shaping mating systems. However, no study has clearly separated the direct effect of having multiple partners from the indirect effect of having more outbred offspring on the resulting reproductive success of individuals in the wild. In this study, we report significant associations between both multiple mating and within-individual genetic diversity of offspring, and an increased reproductive success of wild female Atlantic salmon, Salmo salar. Specifically, we found that females with a higher number of mates also have more outbred offspring (within-individuals), and that both of these characteristics increased their reproductive success expressed in terms of offspring surviving when combining all freshwater juvenile stages. Our findings also indicate that determinants of fitness are different among sexes as within-individual offspring genetic diversity was not a strong predictor of male reproductive success, while the number of mates was important. We also show that females mated with more outbred males than on average, which potentially increased their chances of producing outbred offspring. These results therefore suggest that there could be more important indirect genetic benefits of multiple mating for females than for males.Communicated by M. Abrahams     

Tactics, effectiveness and avoidance of mate guarding in the blue-footed booby (Sula nebouxii)

We examined the dynamics and avoidance of mate guarding, by males and females, in the blue-footed booby, in which the two social mates are usually simultaneously present on the territory but each of them is unmonitored by the other for one-quarter of its time. Both sexes were promiscuous and liable to switch mates. Cuckolded individuals did not increase their overall presence on the territory, but in response to the extra-pair (EP) courtships of their mates, both sexes doubled their rate of intra-pair (IP) courtship and sometimes showed aggression. The male or female's presence depressed the social mate's EP activity, but intra-pair courtship had no such effect, tending even to propitiate that EP activity. Similarly, when females responded to their social mates' EP courtship with approach or aggression, disruption of EP activity was short-lived. Promiscuous females modified their diurnal pattern of attendance, as if attempting to sidestep monitoring by their mates, but cuckolded males matched the modification. Both sexes tended to perform their EP activities at a distance when their mates were present, possibly to evade monitoring or disruption by their mates. Male and female boobies cannot monitor their mates continuously, they do little to facultatively adjust their presence on territory to the risk of infidelity, and their immediate responses to overt infidelity have only the briefest impact; but the information they acquire while monitoring their mates may be critical to constraining their mates' infidelity and also to calibrating their own reproductive investment.     

Male mating bias and its potential reproductive consequence in the butterfly <Emphasis Type="Italic">Colias eurytheme</Emphasis>

Male mating biases may be a widespread feature of animal mating systems but the phenotypic consequences of these biases are often unclear, especially in species for which the operational sex ratio is strongly male-biased. In Colias butterflies, male choice is thought to be one of the factors responsible for maintaining a female-limited genetic color polymorphism, in which female wings appear either yellowish-orange or white (the “alba” variant). Previous studies have indicated that alba females of two montane Colias species mate fewer times during their lifetime, possibly as a partial consequence of this bias. Here we report the results of a field study of male mating behavior and female mating biology in Colias eurytheme, conducted under conditions of high (summer) and low (spring) population densities. Our data show that despite a substantial male bias in approaching alba vs yellowish-orange phenotypes [ratios of 0.08:1 (spring) and 0.28:1 (summer)], alba females did not contain, on average, fewer or smaller spermatophores. Not one of the 308 sampled females was virgin, but females of both phenotypes accumulated spermatophores with age, and tended to carry fewer, larger spermatophores in spring. These data suggest that significantly fewer (or lighter) spermatophores need not be an obligatory or simple consequence of a strong male bias in butterflies. We discuss these findings in light of the known, thermally and density-dependent complexities of alba reproductive biology and of the Colias mating system.     

Partial compensation of the sublethal effect of deltamethrin on the sex pheromonal communication of Trichogramma brassicae

Pyrethroid insecticides are widely used and lead to a sizable environmental pollution that could interfere with the population biology of insects. Trichogramma is a beneficial insect used in biological control and which natural populations contribute to the control of Lepidopterus pests. In this work, we determined the effect of a sublethal dose of deltamethrin on the sex pheromonal communication of Trichogramma. The dose used (LD 0.1) induces no detectable mortality (the theoretical mortality is only one insect over 1000) and can be a good representation of contamination by this insecticide from environmental pollution. The insecticide was shown to have opposite effects on the sex pheromonal communication of Trichogramma, depending on which sex was exposed (Delpuech, J.M., Legallet, B., Terrier, O., Fouillet, P., 1999. Chemosphere 38, 729–739). We show that, when both sexes are simultaneously exposed to the insecticide, this effect is only partially neutralized. The mean response of treated males responding to the sex pheromone from treated females is not significantly different from that of controls, but the kinetics of their response is not the same. When both sexes are treated, the response of males to the sex pheromone is lower at the beginning but their response does not decrease during time contrary to controls and becomes finally higher than that of controls. Therefore, the sublethal effect of deltamethrin in the field can be either advantageous or disadvantageous depending on the difficulty in finding females and their scarcity.     

Reproductive rates,operational sex ratios and mate choice in St. Peter’s fish

Operational sex ratio (OSR) theory predicts that sexual differences in potential reproductive rates (PRRs) create biases in the OSR and thus determine the relative strength of sexual selection (competition and choice) operating on each sex. Although this theory is well accepted, empirical studies that quantify it are still lacking. This paper presents such a study. I measured the natural OSR of Galilee St. Peter’s fish (Sarotherodon galilaeus) in the field (Lake Kinneret) and examined the direction of mate choice in the laboratory. The OSR in Lake Kinneret was male biased. Both a male-biased sex ratio and higher male reproductive rates (twice as fast as females) contributed to the skew in the OSR, but the sexual differences in PRR were shown to be the main factor causing variation in the OSR. Females, the sex with the lower PRR, were more selective for mates. The faster male reproductive rate may explain why females are more selective for mates despite varying less in quality. Received: 29 May 1995/Accepted after revision: 13 April 1996     

Sex allocation in a monomorphic seabird with a single-egg clutch: test of the environment, mate quality, and female condition hypotheses

Sex allocation theory posits that mothers should preferentially invest in sons when environmental conditions are favorable for breeding, their mates are of high quality, or they are in good body condition. We tested these three hypotheses in rhinoceros auklets (Cerorhinca monocerata), monomorphic seabirds that lay a single-egg clutch, in 2 years that differed in environmental conditions for breeding. Results supported the environment and mate quality hypotheses, but these effects were interactive: offspring sex was independent of paternal traits in the poor year for breeding, while females mated to larger and more ornamented males reared more sons in the better year. Conversely, offspring sex was unrelated to female condition, as indexed by hatching date. We propose that good rearing conditions enable females to rear sons possessing the desirable phenotypic attributes of their mates. Results also supported two critical assumptions of sex allocation theory: (1) dimorphism in offspring condition at independence: daughters fledged with higher baseline levels of corticosterone than sons and (2) differential costs of rearing sons versus daughters: mothers rearing sons when environmental conditions were poor completed parental care in poorer condition than mothers rearing daughters in the same year and mothers rearing either sex when conditions were better. These novel results may help to explain the disparate results of previous studies of avian sex allocation.