Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus)

The aim of this study was to investigate reproductive strategies and their consequences in gray mouse lemurs (Microcebus murinus), small solitary nocturnal primates endemic to Madagascar. Previous reports of sexual dimorphism in favor of males and females, respectively, a high potential for sperm competition and pheromonal suppression of mating activity among captive males, led us to investigate mechanisms of intrasexual competition in a wild population. Based on 3 years of mark-recapture data, we demonstrate that sexual dimorphism in this species fluctuated annually as a result of independent changes in male and female body mass. Male body mass increased significantly prior to the short annual mating season. Because their testes increased by 100% in the same period and because their canines are not larger than those of females, we suggest that large male size may be advantageous in searching for estrous females and in enabling them to sustain periods of short-term torpor. In contrast to reports from captive colonies, we found no evidence for two morphologically distinct classes of males. Finally, we also show that most adult males are active throughout the cool dry season that precedes the mating season, whereas most adult females hibernate for several months. This is in contrast to other solitary hibernating mammals, where males typically emerge 1–2 weeks before females. Thus, this first extended field study of M.␣murinus clarified previous conflicting reports on sexual dimorphism and male reproductive strategies in this primitive primate by showing that their apparent deviation from predictions of sexual selection theory is brought about by specific environmental conditions which result in sex-specific life history tactics not previously described for mammals. A general conclusion is that sexual selection can operate more strongly on males without resulting in sexual dimorphism because of independent selection on the same traits in females. Received: 6 July 1997 / Accepted after revision: 28 March 1998     

Mate replacement in experimentally widowed collared flycatchers (Ficedula albicollis): determinants and outcomes

There is increasing evidence that sexual selection may be intense even in socially monogamous birds, resulting from both mate choice and sperm competition. We studied these two modes of sexual selection experimentally by removing paired male collared flycatchers, Ficedula albicollis, from their mates for 2 days and investigating the factors that influenced the likelihood of a replacement male appearing and how the removals influenced paternity. Replacement males (usually neighbouring males) appeared at 81% (n = 37) of nests where males were removed. The likelihood of this appearance was unaffected by the probable reproductive value of the female's clutch to the replacing male. A replacement was, however, less likely when the original male had a large forehead patch, a trait previously shown to be subject to sexual selection in this population. Experimental removal of males increased the level of sperm competition: 74% of experimental broods were multiply sired, compared to 29% of unmanipulated broods in a previous study. Only two factors predicted how paternity was shared between males: removed males fathered more young if removed closer to laying, and if they had larger forehead patches. The former result is consistent with last-male sperm precedence determining paternity, whereas the latter adds to other evidence that forehead patch size is the target of female preference in this species. Our results suggest that females exert some control over male replacement, and also that they may influence the fertilisation success of males by behavioural means. Received: 15 July 1998 / Received in revised form: 16 March 1999 / Accepted: 28 March 1999     

Phenotypic manipulation reveals sexual conflict over precopula duration

Sexual conflict is common in nature, but detailed behavioral studies on the role female resistance behavior plays in shaping mating patterns are rare. I manipulated female resistance to examine its effects on pairing dynamics in two ecologically different freshwater amphipods. I found evidence for female behavior playing a role in both the outcome of pre-pairing interactions and the initiation of pairing in both species. In these species, the male optimum pairing duration is greater than the value preferred by females or compromised pairing durations observed under natural conditions, thus indicating sexual conflict. Furthermore, the proportion of male–female encounters producing male grasping was greater and the duration of such interactions was longer when female resistance was reduced. Thus, sexual conflict over pairing duration may select simultaneously for female resistance and for male persistence both of which mediate the outcome of pre-pairing interactions in Hyalella. Contact precopulatory mate guarding and the interactions that precede it are common components of crustacean and insect mating systems, suggesting that such conflicts may play an important role in the evolution of mating traits in many taxa.     

Testosterone is involved in acquisition and maintenance of sexually selected male plumage in superb fairy-wrens, Malurus cyaneus

Testosterone has been proposed as a physiological link between the level of sexual signalling and male condition. Bright plumage is one of the most noticeable sexual signals and is often used by females as a basis for mate choice. Yet bright male plumage is not necessarily testosterone dependent. We investigated the role of testosterone in the moult into seasonal nuptial plumage in male superb fairy-wrens. Early pre-nuptial moult is under intense intersexual selection and males can acquire the bright plumage any time between autumn and the next spring. Testosterone was always undetectable or very low in males in dull eclipse plumage. During the pre-nuptial moult, both the number of males with detectable testosterone and average testosterone levels increased sharply. High testosterone was more correlated with nuptial plumage than with presence of the cloacal protuberance (indicative of sperm storage). Subcutaneous testosterone implants always induced the pre-nuptial moult within 2–3 weeks after implantation, even well outside the natural time range of moulting. Moreover, removal of the implants before the nuptial plumage was completed, arrested the moult process. The evidence suggests that development of the nuptial plumage is testosterone dependent, although we cannot exclude that testosterone exerts its action after conversion to a metabolite such as oestrogen. Once the nuptial plumage was completed, all males maintained substantially elevated testosterone, sometimes months before the onset of breeding. These high levels could be necessary to maintain the plumage, and/or are involved in courtship displays. The results are discussed with respect to potential costs involved in acquiring and maintaining the nuptial plumage. Received: 17 January 2000 / Received in revised form: 24 February 2000 / Accepted: 25 February 2000     

Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets

Recent models of the evolution and dynamics of family structure in cooperatively breeding vertebrates predict that the opening of breeding vacancies in cooperatively breeding groups will result in (1) dispersal movements to fill the reproductive position, and (2) within-group conflict over access to reproduction. We describe the behavioral and demographic changes that followed the creation of breeding vacancies in three wild groups of cooperatively breeding common marmosets (Callithrix jacchus). Replacement of the breeding female was rapid when no adult females remained in the group, but did not occur for several months when other adult females were present. Aggression of adult animals towards same-sex potential immigrants was associated with a period of reduced affiliation, increased intragroup agonism, no intragroup sexual behavior, and frequent extragroup copulations. This ended with the fissioning of groups along sexual lines. After replacement, multiple males copulated with multiple females and vice versa, with no increases in sexually related aggression. Female-female conflict was resolved through infanticide. The lack of direct conflict between males is consistent with cooperative polyandry. After a breeding vacancy appeared, marmoset groups showed conflict of interests among group members similar to those shown by cooperatively breeding birds, but they used different behavioral mechanisms to resolve those conflicts. Our data provide important evidence from a cooperatively breeding mammal to support Emlen’s model for the evolution of vertebrate families, but they suggest that species-specific inter- and intrasexual competitive strategies should be considered before the model can be applied to other cooperatively breeding vertebrates. Received: 23 November 1999 / Received in revised form: 28 March 2000 / Accepted: 1 April 2000     

Potential direct fitness consequences of ornament-based mate choice in a butterfly

Female mate choice has been shown to provide direct mating benefits in several animal groups. In butterflies, for which there are increasing reports of fine-scale color-based mate choice, the evolutionary benefits that accrue from such mating biases, if any, are largely unknown. We addressed this issue in the butterfly Colias eurytheme, a species in which females choose mates on the basis of iridescent ultraviolet (UV) wing ornamentation and in which males donate reproductively beneficial nuptial gifts. In the first experiment, we assessed the mass of gifts donated to 77 virgin females by males sampled directly from a field encounter site. Despite large variance in the male adult phenotype and ejaculate, no single aspect of dorsal wing coloration, including UV brightness, chroma, or hue, was related to ejaculate mass. There was, however, an interesting interaction between the effects of male body size and copula duration upon ejaculate mass, with size scaling positively with ejaculate mass among males involved in shorter copulations (those lasting <70 min) but negatively among males in longer copulations. In the second experiment, we assessed the lifetime fecundity, fertility, and longevity of 85 females mated under similar circumstances to free-flying wild males. Although several wing color parameters proved subtly informative in more sophisticated multivariable models, no model predicted more than about 20% of the variation in any single female fitness parameter. The duration of copulation, which ranged from 35 min to over 16 h and which carries putative costs for females, was, again, only very weakly predicted by male wing color parameters (i.e., R ² = 0.089). Given the overall minor predictive power of male wing coloration in general and of UV brightness in particular, our results do not strongly support the hypothesis that female C. eurytheme prefer bright UV males to obtain direct benefits or to minimize the costs associated with lengthy copulations.     

Carotenoid-based ornamentation as a dynamic but consistent individual trait

Carotenoid-based ornaments act as signals of quality in many animal species. In contrast to feathers, which are relatively stable structures, carotenoid-pigmented integuments (e.g. bills, lores, tarsi) can change colour rapidly and may better reflect changes in physiological condition. I studied the seasonal variations in plasma carotenoids in red-legged partridges (Alectoris rufa) kept on a constant diet and free of intestinal parasites. Furthermore, I analyzed whether seasonal changes in circulating carotenoids were mirrored by the carotenoid-based coloration of eye rings and bill of this species. Plasma carotenoids showed seasonal variation, with higher levels coinciding with the end of the mating and the start of the laying season. Eye ring pigmentation was related to plasma carotenoid levels, and changes in bill hue (but not changes in UV or red bill chroma) mirrored the variation in plasma carotenoids during the breeding season. Despite the seasonal variation, individual differences in eye ring pigmentation and bill hue, UV and red chroma were consistent throughout the breeding season. Similarly, individual differences in eye ring pigmentation and bill hue and red chroma remained consistent between consecutive years. These results suggest that carotenoid based integumentary colorations act as dynamic traits that accurately reflect the carotenoid-status of individuals, thus reliably indicating consistent differences in individual quality. Furthermore, variability in signal expression appears to have a relevant genetic/phenotypic basis independently of environmental conditions. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Phenotypic correlates and survival consequences of male mating success in lek-mating greater prairie-chickens (<Emphasis Type="Italic">Tympanuchus cupido</Emphasis>)

Female choice and male–male aggression are two modes of sexual selection that can lead to elaboration of male morphological and behavioral traits. In lek-mating species, male mating success is often strongly skewed, and it is puzzling why variation in male traits is still observed given directional female choice. If male traits correlated with reproductive success are honest signals of male quality, there may be survival costs associated with the expression of those traits. In this study, we examined whether morphological, behavioral, and territorial traits are correlated with male mating success and survival in the lek-mating greater prairie-chicken (Tympanuchus cupido). We introduce a novel application of multinomial discrete choice models for analysis of female mate choice behavior. We found that behavioral and territorial attributes showed 6.5 times more variability among males than morphological traits. Both display and aggressive behaviors were strong predictors of male mating success, suggesting that both female choice and male–male aggression were important in determining mating success among male greater prairie-chickens. Moreover, annual survival of male prairie-chickens was independent of mating success and male traits. Females appear to be choosing males based on behavioral traits where large variation exists between males (coefficient of variation >30%). Behavioral traits were the most important factor in determining mating success of male prairie-chickens, but the mechanism underlying this relationship is unknown. In the future, experimental manipulations of male hormones or parasite loads could bridge the proximate mechanisms and ultimate consequences of factors mediating male mating success in lek-mating grouse.     

Maintenance of variance in sperm transfer rates in a scorpionfly: food availability,genetic basis,and heritability

Variation in traits closely related to fitness is expected to be low. This is because these traits are under directional selection and the best genotype should prevail. However, there have been a number of studies demonstrating the existence of considerable variance in sexually selected traits, which is generally known as the lek paradox. Accordingly, earlier studies found substantial variation in sperm transfer rates in Panorpa vulgaris. Aiming at finding the mechanism that maintains this variation, we analyzed the condition dependence and the narrow sense heritability of sperm transfer rates. Food deprivation in the larval/adult phase caused a decrease in the males’ capability of saliva secretion resulting in shorter copulations and a reduced number of transferred sperm. There was a positive correlation between mean sperm transfer rates and mean body mass. Additionally, intermale variation in sperm transfer rates decreased with increasing food availability. Hence, we suggest that sperm transfer rates in P. vulgaris are influenced by adult feeding history. Heritability analyses of sperm transfer rates did not provide significant results, which is consistent with the general hypothesis that additive genetic variance in traits closely related to fitness is small. Since a trait’s potential to respond to selection is proportional to the amount of contained additive genetic variance, the ascertained small heritability provides a satisfying explanation for the maintenance of substantial variation in sperm transfer rates.     

Testosterone and melanin-based black plumage coloration: a comparative study

Despite the functional significance of melanin-based plumage coloration in social and sexual signaling, the mechanisms controlling its information content are poorly understood. The T-regulation hypothesis proposes that melanin ornaments signal competitive abilities via the effects of testosterone (T) mediating both melanization and sexual/aggressive behaviors. Using the phylogenetic comparative approach, we tested whether frontal black melanization is associated with elevated T around the time of breeding plumage development across all bird species with available T-data. We found a context-dependent relationship between melanization and T, varying with the type of ornamentation (patchy or full-black) and with the presumed taxonomic distribution of the hormonal control of plumage dichromatism. Within two taxa in which male plumage development is assumed androgen-dependent (Charadriiformes, Corvida), evolutionary increases in male melanization, and melanin dichromatism correlated with increases in T in most analyses but not within the basal lineage (ratites, Galloanseriformes) with androgen-independent male plumage. Among Passeroidea with presumably genetically or luteinizing-hormone-based male plumage, melanization and its dichromatism correlated with T only in species with <100% frontal melanization. These results were robust as we controlled for several confounding variables such as mating and parental behaviors. This study is the first to test and support the T-regulation hypothesis interspecifically, suggesting that among-species differences in melanization may have evolved in response to differences in circulating T in certain avian taxa. Our results imply that the extent of black ornamentation may serve as an honest indicator of male competitiveness in those species that evolved an appropriate hormonal basis (T dependence) for color production. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.