Secondary sexual characters and female quality in primates

Honest advertisement models of sexual selection propose that exaggerated secondary sexual ornaments are condition-dependent, and that only individuals with superior disease resistance will be able to express costly ornamentation. Studies of secondary sexual ornamentation and their maintenance by sexual selection tend to focus on males. However, females may also possess showy ornaments. We investigated whether female ornaments, in the form of sexual swellings, reliably signal female fitness in a semifree-ranging colony of mandrills (Mandrillus sphinx) at the Centre International de Recherches Médicales, Franceville (CIRMF), Gabon. We measured swelling height and width using photographs of periovulatory females over three mating seasons and compared swelling size with parasitism (using fecal analysis over one annual cycle), immune status (ratio of lymphocytes to neutrophils in blood smears made during captures), and genetic diversity (microsatellite heterozygosity). Swelling size varied by up to 10% between cycles in individual females, giving some support to the hypothesis that size differences may indicate the quality of individual swelling cycles. However, there was no significant difference in swelling size between conceptive and nonconceptive cycles. Measures of swelling size varied more between females than within females across swelling cycles, implying that swelling size was a relatively consistent characteristic of individual females. Swelling size was not significantly related to either general measures of parasitism and immune status, or to the closest available measures to each swelling cycle. Nor was swelling size significantly related to genetic diversity. The healthy, provisioned nature of the colony and problems associated with observational, correlational studies restrict interpretation of our data. However, in combination with previous findings that females of higher reproductive success do not show larger swellings, and that males do not allocate mating effort as a function of swelling size, these results imply that sexual swelling size does not indicate female quality in these semifree-ranging mandrills.     

Size of sexual swellings reflects ovarian function in chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

While many theories exist on the evolution of the sexual swelling signal in female primates, the significance of the very large and variable swellings found in some catarrhine primates is still debated. As suggested by Pagel [(1994) Anim Behav 47:1333–1341], these exaggerated and costly signals have the potential to provide information about differential female reproductive quality to males. While Domb [(2000) Department of Anthropology, Harvard University, Cambridge] and Domb and Pagel [(2001) Nature 410:204–206] propose that swellings serve to reliably indicate between-female fitness differences, we hypothesize that they may indicate current reproductive cycle quality, within or between females. This study examines the between-cycle relationship between ovarian function, gauged via fecal steroid analysis, and absolute size of sexual swellings, yielded through photogrammetric methods. Fourteen cycles from eight captive, group-living chimpanzees (Pan troglodytes) exhibited considerable variability both in ovarian steroid levels and maximum sexual swelling size. Nearly all measures of a female's maximal swelling in a cycle correlated with early follicular and early luteal estradiol averages and the duration of luteal progesterone elevation. Swelling area was also correlated with late follicular estradiol. Given past evidence that such measures of ovarian function predict conceptive success, these data strongly suggest that swellings could convey information to competing males about the fecundability of a potential mate.Communicated by C. Nunn     

Influence of growth on reproductive traits and its effect on fertility and gene diversity in a clonal seed orchard of scots pine, Pinus Sylvestris L

This study was carried out in a clonal seed orchard of scots pine (Pinus sylvestris L.), to determine the difference and interaction for reproductive and growth characters among clones and its impact on fertility variation and gene diversity Numbers of female and male strobili, and height and diameter at breast height were studied on six grafts chosen randomly in each of the 27 clones for the purpose. One-way analysis of variance revealed large differences in both reproductive and growth characters among clones. The differences were higher in growth characters than in reproductive traits. There was significant phenotypic correlation among growth and reproductive characters. So, growth characters had a greater effect on male and female fertility Estimates of total fertility variation (Sibling coefficient = 1.012), status number (26.8) and relative gene diversity (0.981) were computed. Fertility variation among clones was low, which caused a high relative population size (99% of census number). The positive phenotypic correlation between growth and reproductive characters showed that enhanced growth rate could be effective in improving fertility and gene diversity of seed orchard crop. The results of the study have implications in breeding and selection of plus tree and populations, establishment and thinning of seed orchards of the species.     

Dominance rank,resource availability,and reproductive maturation in female savanna baboons

Summary Ten years of data collected from a population of savanna baboons, Papio cynocephalus anubis, residing near Gilgil, Kenya were analyzed to ascertain the extent to which social and ecological factors influence reproductive maturation in females. First sexual swelling occurred at an average age of 4.79 years and first birth occurred at an average age of 6.92 years. Age at first menses was significantly correlated with age at first sexual swelling, but age at first sexual swelling was not a good predictor of age at first birth. The amount of rainfall in the 6 months preceding first sexual swelling and resource availability were significantly correlated with age at first sexual swelling. When ecological factors were taken into account, dominant females had an earlier age at onset of puberty, but not an earlier age at first birth, than did subordinate females. We suggest that nutritional and social stress operate at the same physiological level to disrupt GnRH pulsatility and retard reproductive maturation in some females. Given that socioecological variables modify the timing of life history events related to fitness in female baboons, the task for the future is to unravel how socioecological factors influence different life history components and generate variation in lifetime reproductive success. Correspondence to: F.B. Bercovitch     

The evolution of female social relationships in nonhuman primates

Considerable interspecific variation in female social relationships occurs in gregarious primates, particularly with regard to agonism and cooperation between females and to the quality of female relationships with males. This variation exists alongside variation in female philopatry and dispersal. Socioecological theories have tried to explain variation in female-female social relationships from an evolutionary perspective focused on ecological factors, notably predation and food distribution. According to the current “ecological model”, predation risk forces females of most diurnal primate species to live in groups; the strength of the contest component of competition for resources within and between groups then largely determines social relationships between females. Social relationships among gregarious females are here characterized as Dispersal-Egalitarian, Resident-Nepotistic, Resident-Nepotistic-Tolerant, or Resident-Egalitarian. This ecological model has successfully explained differences in the occurrence of formal submission signals, decided dominance relationships, coalitions and female philopatry. Group size and female rank generally affect female reproduction success as the model predicts, and studies of closely related species in different ecological circumstances underscore the importance of the model. Some cases, however, can only be explained when we extend the model to incorporate the effects of infanticide risk and habitat saturation. We review evidence in support of the ecological model and test the power of alternative models that invoke between-group competition, forced female philopatry, demographic female recruitment, male interventions into female aggression, and male harassment. Not one of these models can replace the ecological model, which already encompasses the between-group competition. Currently the best model, which explains several phenomena that the ecological model does not, is a “socioecological model” based on the combined importance of ecological factors, habitat saturation and infanticide avoidance. We note some points of similarity and divergence with other mammalian taxa; these remain to be explored in detail. Received: 30 September 1996 / Accepted after revision: 20 July 1997     

Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds

Pinnipedia contains some of the most spectacular examples of sexual size dimorphism, examples that are therefore frequently used to illustrate the theory of sexual selection. This paper addresses the question of whether a significant relationship between sexual selection and size dimorphism exists in a comparative context. Thus, harem size and body size data gathered from the literature were analysed with independent contrasts analyses. These investigations showed that sexual size dimorphism is not a consequence of an allometric relationship between male and female size. Instead, there is a clear relationship between harem size and sexual size dimorphism. Further analyses also revealed a significant relationship between harem size and male size whereas no such relationship existed for females. These results support the hypothesis that sexual size dimorphism in pinnipeds is the product of an exclusively male response to sexual selection.     

Sex-biased lactational duration in a human population and its reproductive costs

Summary We tested the proposition that among humans (1) differences in lactational duration result in differences in costs of reproduction even under rich nutritional conditions; and (2) elimination of factors postulated to favor male-biased parental care will be reflected in elimination or reversal of sex-biased care. To do so, we examined the relationship between lactational duration and fertility among Hutterites, a communal-living human population in which the levels of nutritional resources and fertility are high, breast-feeding is the norm, contraceptive use is limited and the collective social and economic system results in low resource variance among individuals. We demonstrate that even under good nutritional conditions, duration of nursing was a significant predictor of the length of time to next pregnancy and that nursing continued to suppress fertility after the resumption of menses. Moreover, we find that daughters were nursed longer than sons, leading to a longer interval to next pregnancy. We examine this uncommon, but not unique, finding of female-biased human parental care in the light of Hutterite social structure, and we explore the consistency of this finding with the most applicable models of parental investment. Correspondence to: S.W. Margulis     

Ecological drivers of group living in two populations of the communally rearing rodent, Octodon degus

Intraspecific variation in sociality is thought to reflect a trade-off between current fitness benefits and costs that emerge from individuals' decision to join or leave groups. Since those benefits and costs may be influenced by ecological conditions, ecological variation remains a major, ultimate cause of intraspecific variation in sociality. Intraspecific comparisons of mammalian sociality across populations facing different environmental conditions have not provided a consistent relationship between ecological variation and group-living. Thus, we studied two populations of the communally rearing rodent Octodon degus to determine how co-variation between sociality and ecology supports alternative ecological causes of group living. In particular, we examined how variables linked to predation risk, thermal conditions, burrowing costs, and food availability predicted temporal and population variation in sociality. Our study revealed population and temporal variation in total group size and group composition that covaried with population and yearly differences in ecology. In particular, predation risk and burrowing costs are supported as drivers of this social variation in degus. Thermal differences, food quantity and quality were not significant predictors of social group size. In contrast to between populations, social variation within populations was largely uncoupled from ecological differences.     

No relationship between long-distance acoustic mate attraction signals and male fertility or female preference in spring field crickets

To father offspring, a male must succeed at two processes of sexual selection: (1) mate with a female and (2) fertilize her eggs. We investigated the relationships between pre- and post-copulatory male traits and female mating responses in wild-captured and laboratory-reared spring field crickets, Gryllus veletis. The phenotype-linked fertility hypothesis suggests that females may receive a direct benefit, enhanced fertilization efficiency, by mating with males that signal attractively. We measured fine-scale components of male acoustic mate attraction signals as well as how much time males spent signalling, measured female preference for males in mating trials and then quantified sperm number and viability. We found no relationship between male signalling traits and male fertility or female preference, providing no evidence for the phenotype-linked fertility hypothesis. We also found no difference in sperm metrics between wild-captured and laboratory-reared males. While female crickets may receive benefits by choosing males based on acoustic signal characteristics, whether the benefits are a result of genetic quality, seminal fluid contents or some other male trait remains unknown.     

Variation among populations of the sailfin molly in the rate of concurrent multiple paternity and its implications for mating-system evolution

We examined patterns of concurrent multiple mating in a live-bearing poeciliid fish, the sailfin molly (Poecilia latipinna). We tested whether the probability of multiple paternity was related to female body size or fertility and whether the rate of multiple paternity varied among four populations that differed in their distributions of female body size and fertility. We analyzed data on mother and offspring genotypes for three polymorphic allozymes by three techniques, including a maximum-likelihood estimator that accounts for sampling error in both parental and offspring allele frequencies. The estimated rate of multiple paternity varied between 0.09 and 0.85, and the rate in one population varied seasonally between 0.33 (spring) and 0.85 (autumn). The variation in these rates was not associated with variation in body-size distributions among populations but was closely associated with variation in size-specific fertility: populations with greater variation in female fertility had higher multiple-paternity rates. Within two populations, logistic regression revealed that individual females of larger body size and greater size-specific fertility were more likely to carry multiply sired broods. This result is consistent with observations made in one of the populations 5 years earlier. In general, the results strongly suggest that the mating system varies markedly among conspecific populations of sailfin mollies and that larger, more fertile females are the objects of intermale competition. Received: 6 May 1996 / Accepted in revised form: 5 December 1996     

Strategic male signalling effort in a desert-dwelling fish

Males often use elaborate courtship displays to attract females for mating. Much attention, in this regard, has been focused on trying to understand the causes and consequences of signal variation among males. Far less, by contrast, is known about within-individual variation in signal expression and, in particular, the extent to which males may be able to strategically adjust their signalling output to try to maximise their reproductive returns. Here, we experimentally investigated male courtship effort in a fish, the Australian desert goby, Chlamydogobius eremius. When offered a simultaneous choice between a large and a small female, male gobies spent significantly more time associating with, and courting, the former, probably because larger females are also more fecund. Male signalling patterns were also investigated under a sequential choice scenario, with females presented one at a time. When first offered a female, male courtship was not affected by female size. However, males adjusted their courtship effort towards a second female depending on the size of the female encountered previously. In particular, males that were first offered a large female significantly reduced their courtship effort when presented with a subsequent, smaller, female. Our findings suggest that males may be able to respond adaptively to differences in female quality, and strategically adjust their signalling effort accordingly.     

Variation in signal timing behavior: implications for male attractiveness and sexual selection

Mate choice often takes place in group settings, such as leks or choruses, in which numerous individuals display and compete for mates simultaneously. In addition to well-known preferences for male traits like size and signaling rate, females of group-displaying species often show preferences that are based on the relative timing of male signals, generally preferring the leading signal. Variation in male signal timing behavior may therefore affect male attractiveness and, ultimately, reproductive success. I used acoustic communication in green treefrogs (Hyla cinerea) to assess the amount of signal timing variation found in natural choruses and to test hypotheses about the sources of variation in signal timing behavior. I recorded dyads of vocally interacting males in the field to describe patterns of variation in signal timing behavior. Incorporating information about female signal timing preferences, I also assessed the amount of variation in signal timing that is likely to be selectively neutral, as well as the amount that is likely under selection by female choice because it involves attractive or unattractive signal placement. I show that there is considerable variation in signal timing behavior, particularly involving neutral signal timing placement. I also show that between-male variation in other traits (size, signal period) is partly linked to variation in signal timing behavior and discuss these findings in terms of male attractiveness and sexual selection in group-displaying organisms.     

Pheromone-based female mate choice and its effect on reproductive investment in a spitting spider

Numerous studies have focused on whether organisms can signal or perceive pheromones and use chemical signals in species and mate recognition. Recently, there have been an increasing number of studies investigating whether pheromones are used in mate choice. Yet, little attention has been paid in exploring the effects of pheromone-based mate choice on reproductive investment. We first tested this hypothesis by providing virgin Scytodes sp. females with a choice between two virgin males in the presence of chemical signals alone and found strong evidence of an odor-based mate preference. We then examined the consequences of the odor-based mate choice by allowing female Scytodes sp. that had previously made an odor-only mate choice to mate with preferred and non-preferred males, respectively. We measured the success of copulation, mortality of male, pre-oviposition interval, egg-sac weight, egg weight, fecundity, fertility, embryonic period, and size of offspring at hatching. Females that mated with the preferred males produced significantly heavier egg sacs that contained more and larger eggs with a greater fertility. Significantly more non-preferred males than preferred males were killed by spitting. However, pre-oviposition interval, embryonic period, and hatchling size were not affected by female mate choice. This study is the first to demonstrate that female spiders are able to regulate their highly valuable reproductive investment based solely on chemical signals.     

Life-history variation in three coexisting cheilostome bryozoan species of the genus Stylopoma in Panamá

Life-history variation was studied in three sympatric species of Stylopoma Levinsen [S. spongites (Pallas), S. projecta Canu and Bassler and Stylopoma n. sp. 15] in Panamá. Bryozoan colonies were collected from 27 reefs along 300 km of the Caribbean coast of Panamá. The distribution and abundance of each species were very patchy, but with broad overlap in occurrence among localities and depths. Nevertheless, species differed considerably in colony size, size at first reproduction and numbers of brooding larvae; implying that interspecific differences in life-history traits may contribute to their coexistence. To examine closely this variation in life-history patterns, we grew, in a common garden experiment, the offspring of the two most common species that were obtained from parent colonies collected from several reefs. There were highly significant differences in growth rates and the timing and extent of sexual reproduction which corresponded well to patterns observed in individuals from the field. Other factors, including size of larvae, extent of secondary zooidal calcification and numbers of avicularia were also correlated with differences in life histories. Despite this additional complexity, however, ecological consequences of trade-offs in life history among modular species such as Stylopoma spp. appear very similar to those among unitary species.     

Sources of variation in male mating success and female oviposition rate in a nonterritorial dragonfly

Summary Variance in male mating success and female oviposition rate was studied on a lifetime and daily scale in a nonterritorial libellulid dragonfly. While controlling for weather, population density, and sex ratio, we investigated whether phenotypic variation could explain a significant amount of the observed variation. By collecting most of the data in a large outdoor field enclosure, we had access to (1) real lifetime data as emigration was prevented, (2) exact values of density and sex ratio, and (3) phenotypic data that are virtually unavailable under natural conditions. Variance in LMS was higher in males than variance in lifetime number of ovipositions in females. Lifespan was of major importance in explaining the variation. Males readily remated on the same day whenever possible (maximum 6 times), whereas in females each oviposition bout usually was followed by a nonreproductive period of approximately 4 days. An analysis of the sources of variance in daily reproduction rate showed that, besides the expected effects of weather, an excess of one sex resulted in a negative effect on the individual mating probability of members of that sex. Even after correction for weather and population parameters, phenotypic traits explained a significant amount of the remaining variation: males with a high mating rate were large, agonistic, active mate searching, and long-living individuals. Females were more likely to oviposit when they showed higher flight activity and when more days had elapsed since the previous oviposition. The presence of a strong size effect on male mating probability, and its absence in females, was confirmed at a pond (native habitat). We propose a model on the causal relationships between the relevant parameters and the variation in reproductive success. Finally, we briefly discuss why variance in reproductive success is not a very good measure of the opportunity for sexual selection in this species. Offprint requests to: N.K. Michiels at the present address     

The development of sex differences in ring-tailed lemur feeding ecology

Sex differences in feeding ecology may develop in response to fluctuations in physiological costs to females over their reproductive cycles, or to sexual size dimorphism, or function to minimize feeding competition within a group via resource partitioning. For most mammal species, it is unknown how these factors contribute to sex differences in feeding, or how the development of males and females reflects these intraspecific feeding differences. We show changes in dietary composition, diversity, overlap, and foraging behavior throughout development in ring-tailed lemurs (Lemur catta) and test how the development of sex differences in feeding is related to female costs of reproduction and year-round resource partitioning. Sex differences in dietary composition were only present when females were lactating, but sex differences in other aspects of feeding, including dietary diversity, and relative time spent feeding and foraging, developed at or near the time of weaning. Sex difference in juveniles and subadults, when present, were similar to the differences found in adults. The low year-round dietary overlap and early differences in dietary diversity indicate that some resource partitioning may begin with young individuals and fluctuate throughout development. The major differences between males and females in dietary composition suggest that these larger changes in diet are closely tied to female reproductive state when females must shift their diet to meet energetic and nutritional requirements.     

Day length,latitude and behavioural (in)flexibility in baboons<Emphasis Type="Italic"> (Papio cynocephalus ursinus</Emphasis>)

Annual cycles in day length are an important consideration in any analysis of seasonal behaviour patterns, since they determine the period within which obligate diurnal or nocturnal animals must conduct all of their essential activities. As a consequence, seasonal variation in day length may represent an ecological constraint on behaviour, since short winter days restrict the length of the time available for foraging in diurnal species (with long summer days, and thus short nights, a potential constraint for nocturnal species). This paper examines monthly variation in activity patterns over a 4-year study of chacma baboons (Papio cynocephalus ursinus) at De Hoop Nature Reserve, South Africa. Time spent feeding, moving, grooming and resting are all significant positive functions of day length, even before chance events such as disease epidemics and climatically mediated home range shifts have been accounted for. These results provide strong support for the idea that day length acts as an ecological constraint by limiting the number of daylight hours and thus restricting the active period at certain times of year. Day length variation also has important implications across populations. Interpopulation variation in resting time, and non-foraging activity in general, is a positive function of latitude, with long summer days at temperate latitudes apparently producing an excess of time that cannot profitably be devoted to additional foraging or social activity. However, it is the short winter days that are probably of greatest importance, since diurnal animals must still fulfil their foraging requirements despite the restricted number of daylight hours and elevated thermoregulatory requirements at this time of year. Ultimately this serves to restrict the maximum ecologically tolerable group sizes of baboon populations with increasing distance from the equator. Seasonal variation in day length is thus an important ecological constraint on animal behaviour that has important implications both within and between populations, and future studies at non-equatorial latitudes must clearly be mindful of its importance.     

Giant pandas attend to androgen-related variation in male bleats

Although androgen-dependant traits are predicted to signal overall male quality, no study has examined the response of a nonhuman animal to variation in a known acoustic cue to male androgen levels (steroid hormones that are key drivers of male sexual behaviour). Here, we use a single-speaker approach to present male and female giant pandas with re-synthesised male bleats representing callers with high and low androgen levels. Our results revealed that male and female giant pandas had significantly greater-looking responses, spent more time pacing, and were faster to respond to playbacks of bleats simulating high androgen males. When we analysed the sexes separately, a slightly different response pattern was revealed: whereas males and females still had significantly greater-looking responses and were faster to respond to bleats simulating high androgen males, only male giant pandas tended to spend more time pacing. These findings suggest that vocal cues to male androgen levels are functionally relevant to male and female giant pandas during the breeding season, and constitute the first demonstration that a nonhuman animal could be using a vocal signal to assess male hormonal state. We go on to discuss the ecological relevance of signalling androgen levels in this species’ sexual communication and the possible application of our results to conservation breeding.     

Asymmetry in a visual signaling character and sexual selection in a wolf spider

Fluctuating asymmetry (FA) can indicate developmental instability in bilaterally symmetric organisms, and studies have shown that the degree of asymmetry in male secondary sexual characters influences female mate choice in a number of taxa. In male Schizocosa ocreata wolf spiders, conspicuous tufts of bristles on the forelegs are a critical component of visual courtship signals, which appear to play a role in female mate choice. Previous studies have shown that females exhibit reduced receptivity to males with regenerative asymmetry, a consequence of leg loss and regeneration that causes males to be grossly asymmetric with respect to this important signaling character. We provide data on the occurrence of FA in the tufts of S. ocreata, and examine further the influence of asymmetry on female mate choice. The distribution of tuft area asymmetry values from a sample of field-collected males was normal, with a mean value of zero, indicating true FA. For a subset of males measured directly after field collection and prior to feeding, tuft asymmetry was significantly negatively correlated with measures of body size (body length) and condition (abdomen volume/cephalothorax width). Receptivity responses of females to visual signals from live males of similar size varied with the degree of asymmetry in male tufts. Since FA covaries with male body size and condition, which may also influence behavioral vigor, we used video image manipulation to alter the degree of asymmetry in tufts of a courting male while holding size and condition constant. Asymmetry treatments represented values within the range of natural FA variation as well as more extreme values characteristic of regenerative asymmetry. With the confounding effects of male size, condition, and behavior held constant, female spiders exhibited reduced receptivity responses to all experimental asymmetric video images relative to a control video stimulus. There were no differences in the frequency of female receptivity among the various asymmetry treatments, suggesting that discrimination against asymmetry in conspecific male signal characters is not simply a rejection of extreme phenotypes. Results suggest that asymmetry in a key male secondary character used in visual signaling, independent of any concomitant behavioral or size factor, is an important criterion in mate choice. Received: 26 February 1998 / Accepted after revision: 12 September 1998