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Influence of the mother's reproductive state on the hormonal status of daughters in marmosets (Callithrix kuhlii).

Behavioral and endocrine suppression of reproduction in subordinate females produces the high reproductive skew that characterizes callitrichid primate mating systems. Snowdon et al. [American Journal of Primatology 31:11-21, 1993] reported that the eldest daughters in tamarin families exhibit further endocrinological suppression immediately following the birth of siblings, and suggested that dominant females exert greater control over subordinate endocrinology during this energetically challenging phase of reproduction. We monitored the endocrine status of five Wied's black tufted-ear marmoset daughters before and after their mother delivered infants by measuring concentrations of urinary estradiol (E(2)), pregnanediol glucuronide (PdG), testosterone (T), and cortisol (CORT). Samples were collected from marmoset daughters 4 weeks prior to and 9 weeks following three consecutive sibling-litter births when the daughters were prepubertal (M=6.1 months of age), peripubertal (M=11.9 months), and postpubertal (M=17.6 months). The birth of infants was associated with reduced ovarian steroid excretion only in the prepubertal daughters. In contrast, ovarian steroid levels tended to increase in the postpubertal daughters. Urinary E(2) and T levels in the postpubertal daughters were 73.8% and 37.6% higher, respectively, in the 3 weeks following the birth of infants, relative to prepartum levels. In addition, peak urinary PdG concentrations in peri- and postpubertal daughters were equivalent to luteal phase concentrations in nonpregnant, breeding adult females, and all of the peri- and postpubertal daughters showed clear ovulatory cycles. Cortisol excretion did not change in response to the reproductive status of the mother, nor did the concentrations change across age. Our data suggest that marmoset daughters of potential breeding age are not hormonally suppressed during the mother's peripartum period or her return to fertility. These findings provide an additional example of species diversity in the social regulation of reproduction in callitrichid primates.

Animals↗

Comparative penile morphology of East African galagos of the genus Galagoides (family Galagidae): implications for taxonomy.

Recent studies on the comparative penile morphology of galagos have revealed complex patterns that vary among both genera and species, and help with species identification. So far the penile morphologies of 14 galago species have been described and an identification key has been proposed. The present study extends and revises previous work. Wild Galagoides cocos, G. granti, G. zanzibaricus and G. rondoensis from the Eastern Arc Mountains and coastal forests of Tanzania and Kenya were live-trapped, and one species (G. orinus) was examined using a museum specimen. Penile morphology was photographed, traced, and described qualitatively. All of the mature males had penile spines. Spines were absent or indistinct in immature males of all of the species. The penile morphologies of G. cocos, G. granti, and G. zanzibaricus are similar in their overall distribution and type of spines, but differ in the shape of the glans penis. Both G. orinus and G. rondoensis have divergent penile morphologies compared to all other galagos, and are probably phylogenetically distinct. The results support other recent morphological and behavioral studies that consider these five galagos to be distinct species. The evolution of the baculum and spines is thought to be linked to sexual selection in multimale mating systems, but the mechanisms involved are not entirely understood. Adult male G. rondoensis appear to display the penile spines by exposing the distal section of the penis.

Animals↗

Intrasexual competition and canine dimorphism in anthropoid primates.

A number of factors, including sexual selection, body weight, body-weight dimorphism, predation, diet, and phylogenetic inertia have been proposed as influences on the evolution of canine dimorphism in anthropoid primates. Although these factors are not mutually exclusive, opinions vary as to which is the most important. The role of sexual selection has been questioned because mating system, which should reflect its strength, poorly predicts variation in canine dimorphism, particularly among polygynous species. Kay et al. (1988) demonstrate that a more refined estimate of intermale competition explains a large proportion of the variation in canine dimorphism in platyrrhine primates. We expand their analysis, developing a more generalized measure of intermale competition based on the frequency and intensity of male-male agonism. We examine the relative influences of predation (inferred by substrate use), female body weight, body-weight dimorphism, diet, and sexual selection on the evolution of anthropoid canine dimorphism. Intermale competition is very strongly associated with canine dimorphism. Predation also has a marked effect on canine dimorphism, in that savanna-dwelling species consistently show greater canine dimorphism than other species, all other factors being held equal. Body-weight dimorphism is also strongly associated with canine dimorphism, though apparently through a common selective basis, rather than through allometric effects. Body weight seems to play only a minor, indirect role in the evolution of canine dimorphism. Diet plays no role. Likewise, we find little evidence that phylogenetic inertia is a constraint on the evolution of canine dimorphism.

Analysis of Variance↗

Genital swelling in females of the monogamous gibbon, Hylobates (H.) lar.

Cyclical changes in the vulvae of five adult lar gibbons (Hylobates [H.] lar) were studied and compared with those of eight lowland gorillas. The results reveal that the gibbons have relatively conspicuous and specialized sexual swellings that alter shape and appearance during the ovarian cycle. At maximum extent, the genital swellings of gorillas are relatively and absolutely smaller than those of gibbons, and lack the distinctive coloration seen in the genital swellings of the smaller apes. We conclude that the female gibbon's sexual swelling is a far more conspicuous and effective signal of estrus status than that of the gorilla, and that this is not explicable in terms of allometry. Previous investigators have pointed to one-male mating systems, monogamous pair-bonding, or an arboreal habitat as reasons that some primates should have less conspicuous signals of estrus than others. Our findings for the gibbon are the reverse of these predictions, and indicate that sexual selection other than by intermale competition for estrous females is implicated in the ultimate causation of the gibbon's swelling. The adaptive value and significance of the female gibbon's sexual signals remain unclear, however.

Animals↗

Sexual dimorphism in large-bodied primates: the case of the subfossil lemurs.

Large body size has evolved repeatedly in the order Primates, not merely among anthropoids but also among prosimians. Whereas high degrees of sexual size dimorphism characterize many of the large-bodied anthropoids, this is not the case for extinct large-bodied lemurs. This paper uses finite mixture analysis and other techniques to ascertain just how much skull length dimorphism might be embedded in the generally unimodal distributions of skull lengths of giant extinct lemurs from single localities, and then compares these results with known skull length dimorphisms in extant lemurs and large-bodied catarrhines. We show that low levels of skull length sexual dimorphism (or none at all) characterize subfossil lemurs, and we explore several possible explanations for this phenomenon. Traditional explanations of sexual size dimorphism generally focus on body size or mating systems. These are not sufficient to explain the variation in sexual dimorphism that can be observed in the order Primates.

Animals↗

Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates.

This study examines statistical correlations between socioecological variables (including measures of group composition, intermale competition, and habitat preference) and the ontogeny of body size sexual dimorphism in anthropoid primates. A regression-based multivariate measure of dimorphism in body weight ontogeny is derived from a sample of 37 species. Quantitative estimates of covariation between socioecological variables and this multivariate measure are evaluated. Statistically significant covariation between the ontogeny of dimorphism and socioecological variables, with the possible exception of habitat preference, is observed. Sex differences in ontogeny are lacking in species that exhibit low levels of intermale competition and are classifiable as species with monogamous/polyandrous mating systems. Among dimorphic species, two modes of dimorphic growth are apparent, which seem to be related to different kinds of group compositions. Multimale/multifemale species tend to become dimorphic through bimaturism (sex differences in duration of growth) with minimal sex differences in growth rate. Single-male/multifemale species tend to attain dimorphism through differences in rate of growth, often with limited bimaturism. Measures of intermale competition may also covary with these modes of dimorphic growth, but the relations among these variables are sometimes ambiguous. Correlations between dimorphic growth and behavioral variables may reflect alternative life history strategies in primates. Specifically, the ways in which risks faced by subadult males are distributed and the relations of these risks to growth rates seem to influence the evolution of size ontogenies. The absence of dimorphic ontogeny in some species can be tied to similar distributions of risk in each sex. In taxa that become dimorphic primarily through rate differences in growth, the lifetime distribution of risks for males may change rapidly. In contrast, males may face a pattern of uniformly changing or stable risk in species that become dimorphic through bimaturism. Finally, much variation recorded by this study remains unexplained, providing additional evidence of the need to specially examine female ontogeny before primate body size dimorphism can be satisfactorily explained.

Analysis of Variance↗

Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax).

We studied patterns of genetic relatedness and paternity in moustached tamarins, small Neotropical primates living in groups of 1-4 adult males and 1-4 adult females. Generally only one female per group breeds, mating with more than one male. Twin birth are the norm. In order to examine the genetic consequences of this mating pattern, DNA was extracted from fecal samples collected from two principal and six neighboring groups. DNA was characterized at twelve microsatellite loci (average: seven alleles/locus). We addressed the following questions: Do all adult males have mating access to the reproductive female of the group? How is paternity distributed across males in a group? Can polyandrous mating lead to multiple paternity? Are nonparental animals more closely related to the breeders than to the population mean? And, are mating partners unrelated? Breeding females mated with all nonrelated males. In at least one group the father of the older offspring did not sire the youngest infant although he was still resident in the group. We also found evidence for multiple paternity in a supposed twin pair. Yet, within each group the majority (67-100%) of infants had the same father, suggesting reproductive skew. Relatedness within groups was generally high (average R = 0.31), although both nonrelated males and females occurred, i.e., immigrations of both sexes are possible. Mating partners were never found to be related, hence inbreeding seems to be uncommon. The results suggest that while the social mating system is polyandry, paternity is often monopolized by a single male per group.

Animals↗

A shrew-sized origin for primates.

The origin of primates has had a long history of discussion and debate, with few ever considering the impact of the original body weight on subsequent primate adaptive radiations. Here, I attempt to reconstruct early primate evolution by considering the initial size of primates as well as the critical functional-adaptive events that had to occur prior to the early Eocene. Microcebus is often viewed as a living model, and thus 40-65 g might represent a practical ancestral weight for the origin of primates. I consider a smaller original body weight, likely 10-15 g in actual size, and I address the biological implications for shrew-sized primates by comparing the behavioral ecology of mouse lemurs, our smallest living primates, to another tiny-sized mammalian group, the shrews (Family Soricidae). Several behavioral and ecological characteristics are shared by shrews and mouse lemurs, and several mammalian trends are evident with decreased size. I suggest that a shrew-sized ancestral primate would have had high metabolic, reproductive, and predation rates, relatively low population densities, and a dispersed and solitary existence with a promiscuous mating system. Although small mammals like shrews provide insights concerning the ancestral size of primates, primate origins have always been tied to arboreality. I assess other potential arboreal models such as Ptilocercus and Caluromys. By combining all of this information, I try to sequence the events in a functional-adaptive series that had to occur before the early Eocene primate radiations. I suggest that all of these important adaptive events had to occur at a small body size below 50 g.

Adaptation, Physiological↗

Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size.

Phylogenetic comparative methods were used to analyze the consequences of sexual selection on canine size and canine size dimorphism in primates. Our analyses of previously published body mass and canine size data revealed that the degree of sexual selection is correlated with canine size dimorphism, as well as with canine size in both sexes, in haplorhine but not in strepsirrhine primates. Consistent with these results, male and female canine size was found to be highly correlated in all primates. Since canine dimorphism and canine size in both sexes in haplorhines were found to be not only related to mating system but also to body size and body size dimorphism (characters which are also subject to or the result of sexual selection), it was not apparent whether the degree of canine dimorphism is the result of sexual selection on canine size itself, or whether canine dimorphism is instead a consequence of selection on body size, or vice versa. To distinguish among these possibilities, we conducted matched-pairs analyses on canine size after correcting for the effects of body size. These tests revealed significant effects of sexual selection on relative canine size, indicating that canine size is more important in haplorhine male-male competition than body size. Further analyses showed, however, that it was not possible to detect any evolutionary lag between canine size and body size, or between canine size dimorphism and body size dimorphism. Additional support for the notion of special selection on canine size consisted of allometric relationships in haplorhines between canine size and canine size dimorphism in males, as well as between canine size dimorphism and body size dimorphism. In conclusion, these analyses revealed that the effects of sexual selection on canine size are stronger than those on body size, perhaps indicating that canines are more important than body size in haplorhine male-male competition.

Animals↗

Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation.

The vasopressin V1a receptor is a gene known to be central to species differences in social behavior, including differences between the monogamous prairie vole and its promiscuous congeners. To examine how individual differences compare with species differences, we characterize variability in the expression of the vasopressin V1a receptor (V1aR) in a large sample of wild prairie voles. We find a surprising degree of intraspecific variation in V1aR binding that does not seem attributable to experimental sources. Most brain regions exhibit differences between upper and lower quartiles that are comparable to differences between species in this genus. Regions that are less variable have been implicated previously in regulating monogamous behaviors, suggesting that the lack of variation at these sites could reflect natural selection on mating system. Many brain regions covary strongly. The overall pattern of covariation reflects the developmental origins of brain regions. This finding suggests that shared mechanisms of transcriptional regulation may limit the patterns of gene expression. Such biases may shape both the efficacy of selection and the pattern of individual and species differences. Overall, our data indicate that the prairie vole would be a useful model for exploring how individual differences in gene expression influence complex social behaviors.

Animals↗

Ontogeny and sexual dimorphism of the sonic motor nucleus in the oyster toadfish.

Male oyster toadfish, Opsanus tau, produce a courtship boatwhistle call and have a larger sound-producing organ than females, who do not boatwhistle . We investigated the possibility of sexual dimorphism in ontogeny of the sonic motor nucleus (SMN) of the toadfish. Brain weight increases for life though the increase decelerates with increasing fish weight. Neuron number, ranging from 760 to 2,888 in the SMN, increases rapidly to about 3 years, more slowly to about 8 years, and then levels off. There are no sexual differences in regressions of brain weight and SMN neuron number against fish size or age. Neuronal soma size in the SMN increases from 8 to 35 micron in average diameter and 67 to 916 micron2 in area over a period of at least 7 years. Males have larger neurons than females (P less than .01). However, males can be separated by inspection into populations with large and small soma sizes. Neuron size is not different between females and males with small somas. Neurons in males with large somas are larger than neurons in females and neurons in males with small somas. Such male dimorphism is reminiscent of other behavioral and morphological dimorphisms , which have led to characterization of males into territorial and satellite forms in certain mating systems.

Air Sacs↗

Oligonucleotide DNA fingerprinting optimized to determine parentage in three beetle species.

Oligonucleotide fingerprinting was performed on three beetle species from different families (Coleoptera: Staphylinidae: Aleochara curtula; Silphidae: Nicrophorus vespilloides; Tenebrionidae: Blaps lethifera) to obtain detailed information on parentage in mating systems. We report variations in the number of hybridizing fragments for the different species depending on the combinations of probes and restriction enzymes used. In addition to conventional multilocus fingerprint patterns, we established a single locus system for A. curtula (GTG5; HinfI) and described an oligolocus system in N. vespilloides (GATA4; HaeIII).

Animals↗

DNA preparation and efficient microsatellite analysis from insect hemolymph.

A simple and time-saving method for DNA preparation for efficient microsatellite analysis is described. The method is based on thermal treatment of only 1-5 microL of insect hemolymph in a Chelex 100-suspension. Since hemolymph withdrawal does not harm the insects, analysis of mating systems, population structure and phylogenetic reconstruction can be conducted with minimal experimental influence.

Animals↗

Genetic and molecular analysis of hybrids in the genus Saccharomyces involving S. cerevisiae, S. uvarum and a new species, S. douglasii.

We have studied the phenomenon of infertility of yeast hybrids obtained with physiological conditions under the control of compatible mating systems. The yeasts investigated are three Saccharomyces species: S. cerevisiae, S. uvarum and a new species, S. douglasii. The diploid hybrids from crosses between these species sporulate well but are essentially infertile. The rare viable spores, one per 10(4) to 10(5) asci, that have been examined carry a complete genome comprised of chromosomes contributed by both parents but invariably have extra chromosomes, i.e. they are generally disomic for at least two or three chromosomes. This observation is consistent with a failure, in meiosis I, of the pairing and disjunction of homologous chromosomes which in most cases results in spores with an incomplete set of chromosomes. This apparent lack of pairing of 'homeologous' chromosomes in meiosis I was analysed in most detail with S. cerevisiae/S. douglasii hybrids. As a genetic tool we studied frequencies of recombination, taking advantage of an S. douglasii breeding stock of some 50 identified mutations in non-switching haploids. Recombination, although markedly reduced, could be observed at both the chromosomal and allelic levels, implying a sporadic pairing in meiosis to allow genetic exchange. Meiotic recombination frequencies were studied for 14 gene pairs and generally found to be reduced ten-fold. Heteroallelic recombination (gene conversion) frequencies were measured at 22 loci and were judged to be reduced at least two- to 100-fold. DNA hybridization experiments with S. cerevisiae gene probes gave results consistent with low DNA sequence homologies between S. cerevisiae and S. douglasii. Moreover, by change, our experiments disclosed another Saccharomyces strain (CBS2908, originally classified as S. cerevisiae) with hybridization patterns identical to S. douglasii except for the hybridization with the Ty transposon probes. Crosses between CBS2908 and S. douglasii yielded diploid hybrids with 80-90% spore viability, thus establishing a second member of the S. douglasii species.

Chromosomes, Fungal↗

Polygynous male starlings allocate parental effort according to relative hatching date

In many polygynous bird species, males allocate most of their parental effort to their primary females' broods. There are several hypotheses that may explain this: the relative reproductive value of the brood, the energetic demand of the brood, the genetic quality of the female and the certainty of fatherhood may all be higher for the primary females' broods. Since these parameters may covary in nature, experiments are necessary to determine their importance. Bigynous male European starlings, Sturnus vulgarispredominantly incubated the eggs and fed the nestlings of their primary females. In an experiment we altered the order in which the clutches hatched by exchanging the primary and secondary females' eggs before hatching. Even though experimental males mostly incubated their primary females' clutches, they predominantly fed the nestlings of the secondary female. Experimental males fed secondary females' nestlings significantly more than control males did. In fact, experimental males invested in their secondary females' broods to the same extent as control males invested in their primary females' broods. This result demonstrates that males use relative brood age to decide how to allocate their parental effort between their broods which has important implications for the evolution of the starling mating system.

Journal Article↗

Mating ecology of the nonpollinating fig wasps of Ficus ingens.

The males of many fig wasps fight fatally for mating opportunities. The concentration of females in space has been proposed as one factor selecting for their aggressive behaviour. We studied the temporal distribution of receptive females to obtain a clearer impression of the operational sex ratio in figs. Females of nonpollinating species emerged from figs over a protracted period of time and this resulted in an extremely male-biased operational sex ratio, conducive to extreme fighting. Since there were so few receptive females at any one time, a male could defend an eclosing female. Consequently, the largest, Otitesella longicauda male in a fig had a much higher mating success than smaller males. This suggests that larger males have a larger fitness advantage than larger females and a Trivers-Willard effect could have important implications for sex allocation. Apterous and seemingly nondispersing males routinely left their figs. Such dispersal can affect both (1) sex allocation by reducing the degree of local mate competition between brothers and (2) male dimorphism by reducing the mating opportunities of males with a dispersing morphology. We show that the wingless digitata males of the Otitesella digitata species group disperse on to leaves close to their natal fig. An extremely male-biased sex ratio resulted in almost all O. longicauda females being mated. These findings suggest that the classical concept of the fig wasp mating system is too simplistic and that important assumptions of sex allocation models are violated. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

Resource presence and operational sex ratio as determinants of copulation duration in the fly Rhagoletis juglandis.

The effects of the interaction between the operational sex ratio (OSR) and a resource (i.e. oviposition site) on mating dynamics have rarely been considered. We examined the effect of the resource presence and its interaction, with the effect of OSR on copulation duration in Rhagoletis juglandis, a tephritid fly species characterized by a resource-defence mating system in which males defend territories on walnut fruit. In this species, copulation duration varies from 30 s to over 1 h and was shown previously to respond strongly to changes in OSR. In the field, short copulations tended to begin and end on fruit, whereas most long copulations generally began on fruit but ended in the foliage, suggesting a possible effect of resource presence on the copulation duration. In laboratory assays of isolated pairs, copulations were significantly shorter in the presence of a surrogate fruit, confirming the effect of resource presence. In another laboratory assay, in which we manipulated OSR independently of resource presence, resource presence and OSR were additive in their effects. Results are discussed in the context of sperm competition theory. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

Postcopulatory sexual selection in Mediterranean fruit flies: advantages for large and protein-fed males.

Previous laboratory studies of Mediterranean fruit flies, Ceratitis capitata (medflies), have identified large size and protein feeding as positive influences on the ability of males to secure copulations. In this study, we investigated whether large and protein-fed males experience additional advantages in terms of amount and distribution of sperm stored by mates. We also examined relationships between copula duration and sperm storage. Mates of large and protein-fed males were more likely to store sperm and to store more sperm than mates of small and protein-deprived males. Probability of sperm storage was associated with copula duration; all copulations lasting less than 100 min failed whereas 98% lasting longer than 100 min succeeded. Copulations involving sperm storage were longer if males were small or protein deprived or if the female was large, although there was no evidence of a relationship between copula duration and total sperm storage. Evidence from related studies suggests that variation in latency until sperm transfer, caused by size and diet, is a likely explanation for varying copula duration. Sperm tended to be stored asymmetrically between the female's two spermathecae, consistent with a mating system in which females maintain isolated populations of sperm from different males and later select between them. Storage was less asymmetric when large numbers of sperm were stored but there was little evidence that male size or diet affected this asymmetry. It is uncertain whether postcopulatory advantages of large and protein-fed male medflies arise from female preferences or male dominance through coercion or force. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗