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Histological characteristics of the uterine endometrium and corpus luteum during early embryogenesis and the relationship to embryonic mortality in the domestic cat.

Pregnancy rates are low and litter sizes generally small when assisted reproduction techniques are used in gonadotropin-treated felid (cat) species. A prerequisite to determining whether or not abnormal morphological changes in the uterine lumen or corpus luteum (CL) are related to this reproductive failure is the documentation of normal histological kinetics during natural embryogenesis. This study characterized the histological changes of the endometrium and ovarian CL during the early stages of preimplantation embryonic development in the naturally estrous, mated queen. The purpose was to 1) develop a system for dating the cat endometrium and CL of early pregnancy; 2) document the frequency of abnormal uterine and CL history under natural mating conditions; and 3) compare histological traits of queens producing good- vs. poor-quality embryos. Naturally estrous, mated queens were ovariohysterectomized at 64 h (n = 8), 76 h (n = 11), 100 h (n = 8), 124 h (n = 7), 148 h (n = 6), or 480 h (n = 8) after first copulation. Embryos collected from oviductal and uterine flushings were graded for quality, and uteri and ovaries were fixed in formalin. Fixed tissue sections were stained and multiple histological traits described for each uterine (endometrial height, endometrial vacuolation, percentage of glandular cells with subnuclear vacuoles, number of mitoses, nuclear-to-cytoplasmic ratio) and ovarian (presence of tertiary follicles, vacuolation of luteal cell cytoplasm, luteal cell shape) sample. Modest histological changes were observed at each time point, and these were documented in detail. The most prominent modifications occurred at 124 h after first copulation and included thickening of the endometrium, straightening of the glands, increased cytoplasmic vacuolation, and increased epithelial height. Of 15 queens failing to produce good-quality embryos, only 4 expressed unusual histological characteristics; and 3 of 25 queens producing only high-quality embryos exhibited abnormal uterine or CL cellular integrity. Therefore, aberrant histological changes are not primarily responsible for failure of the naturally estrous, mated queen to produce good-quality embryos. Furthermore, a normative database now is available to date the endometrium and CL of early pregnancy and to examine the impact of exogenous gonadotropins and assisted techniques on uterine/CL structure and function.

Animals↗

Relationship of circulating steroid hormones, luteal luteinizing hormone receptor and progesterone concentration, and embryonic mortality during early embryogenesis in the domestic cat.

Serum hormones, corpus luteum (CL) progesterone, and CL LH receptors were characterized and interrelated to ovarian follicle and CL number and preimplantation embryo quality/survival in the cat. Blood samples were collected from queens ovariohysterectomized at 64 (n = 7), 76 (n = 11), 100 (n = 8), 124 (n = 7), 148 (n = 6), or 480 (n = 8) h after first copulation (3-times-daily matings on Days 2 and 3 of estrus). Ovarian CL were enucleated, weighed, and bisected; one hemi-CL was assayed for progesterone and the other for LH receptors. Serum was assessed for estradiol-17 beta and progesterone. Serum estradiol-17 beta concentrations did not return (p > 0.05) to baseline approximately 20 pg/ml) until 124 h after first copulation, whereas serum progesterone began to increase (> 1 ng/ml) by 76 h, was elevated (p < 0.05) by 124 h, and continued to rise thereafter. Serum progesterone was highly correlated with CL mass and LH receptor and progesterone concentration (range, r = 0.69-0.82; p < 0.01). CL progesterone and LH receptor concentrations were similar (p > 0.05) at 64 and 76 h, and both increased (p < 0.05) at subsequent time intervals and were correlated closely (r = 0.65; p < 0.01). Although ovarian CL were distinct and well organized by 64 h, pronounced elevations in serum progesterone and CL LH receptors and progesterone did not occur until at least 36 h later. The rapid increase in serum progesterone concentrations between 100 and 148 h was related to accelerated LH receptor synthesis and CL progesterone production and not entirely to enhanced CL growth.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Pattern and source of secretion of relaxin in the reproductive cycle of the spotted hyena (Crocuta crocuta).

Female spotted hyenas are highly masculinized at birth and have no external vagina. Copulation with males and birth of young are accomplished through the central urogenital canal of the clitoris. This unusual adaptation requires remarkable changes in the elasticity of the connective tissues of the clitoris, without which neither copulation nor birth would be possible. We hypothesized that relaxin, a hormone that increases the extensibility of the connective tissues of the uterus and cervix of many other mammalian species, plays a role in the clitoral changes observed in hyenas. Serum relaxin was determined by specific RIA. Relaxin was not detected in serum of males, pubertal or nonpregnant adult females, or ovariectomized females. Immunoactive relaxin was detected in serum of juveniles at the time of initial growth of the urogenital meatus. High concentrations of immunoactive relaxin appeared in the serum of pregnant hyenas in the 2 wk preceding parturition. Immunoassays of extracts of hyena tissues and serum obtained from uterine and ovarian veins indicated that the placenta was the predominant source of relaxin, with possible ovarian contributions. Circulating relaxin decreased promptly following cesarean section near term. We conclude that relaxin secretion coincides with changes in extensibility of clitoral connective tissues 1) during growth of the clitoris in juveniles and 2) near the time of parturition in adults.

Animals↗

Male dwarf chameleons assess risk of courting large, aggressive females.

Conflict between the sexes has traditionally been studied in terms of costs of mating to females and female resistance. However, courting can also be costly to males, especially when females are larger and aggressively resist copulation attempts. We examined male display intensity towards females in the Cape dwarf chameleon, Bradypodion pumilum, in which females are larger than males and very aggressive. We assessed whether aggressive female rejection imposes potential costs on males and whether males vary their display behaviour with intensity of female rejection, female size or relative size differences. Males persisted in courtship after initial female rejection in 84% of trials, and were bitten in 28% of trials. Attempted mounts were positively associated with males being bitten. Males reduced courtship with increased intensity of female rejection. Male courtship behaviour also varied with female size: males were more likely to court and approach smaller females, consistent with the hypothesis that larger females can inflict more damage. These results suggest that, in addition to assessing female willingness to mate, male dwarf chameleons may use courtship displays to assess potential costs of persistence, including costs associated with aggressive female rejection, weighed against potential reproductive pay-offs associated with forced copulation.

Aggression↗

Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding.

Three hypotheses concerning potential genetic benefits of female multiple mating behaviour are evaluated for the common shrew. In a high-density population, many successful copulations took place between individuals estimated to be close relatives (e.g. full or half siblings). Juveniles resulting from such matings tended to be relatively small at weaning, and were generally less likely to survive to sexual maturity than more outbred individuals. Multiple paternity was discovered in eight of nine litters examined. The incidence of matings between close relatives, the cost of inbreeding, and the high incidence of multiple paternity presented are each consistent with the hypothesis that female multiple mating is a strategy to reduce inbreeding. That is, if females cannot always distinguish close kin, then they may copulate with several different males and so reduce the risk that all their offspring will be sired by a close relative.

Animals↗

Overcoming cytoplasmic incompatibility in Drosophila.

The endocellular microbe Wolbachia pipientis infects a wide variety of invertebrate species, in which its presence is closely linked to a form of reproductive failure termed cytoplasmic incompatibility (CI). CI renders infected males unable to father offspring when mated to uninfected females. Because CI can dramatically affect fitness in natural populations, mechanisms that abate CI can have equally large impacts on fitness. We have discovered that repeated copulation by Wolbachia-infected male Drosophila simulans significantly diminishes CI. Repeated copulation does not prevent Wolbachia from populating developing spermatids, but may reduce the time during spermatogenesis when Wolbachia can express CI. This restoration of fertility in premated infected males could have important implications for Wolbachia transmission and persistence in nature and for its exploitation as an agent of biological pest control.

Animals↗

The logic of Ménage à Trois.

Recent studies of socially monogamous species have shown that in many cases females do not copulate exclusively with their pair mates, but are also receptive to other males. The explanation usually given for unfaithful female behavior is that most females are unable to bond with a male they would prefer as genetic father to their offspring. To secure male assistance the female therefore pairs with an available male but also copulates with males of supposedly higher genetic quality. Here we offer an alternative evolutionary explanation for female infidelity, which does not rely upon this 'Good Genes hypothesis of female choice. We show with a simple model that in an evolutionary game between three players, a male, a female and a male lover, solutions exist in which the female can secure more assistance from her mate by being receptive to other males. We conclude that female sexuality can have a decisive role in regulating social behaviour, in which the fertile female is the driving force.

Animals↗

Menstrual cycle variation in women's preferences for the scent of symmetrical men.

Evidence suggests that female sexual preferences change across the menstrual cycle. Women's extra-pair copulations tend to occur in their most fertile period, whereas their intra-pair copulations tend to be more evenly spread out across the cycle. This pattern is consistent with women preferentially seeking men who evidence phenotypic markers of genetic benefits just before and during ovulation. This study examined whether women's olfactory preferences for men's scent would tend to favour the scent of more symmetrical men, most notably during the women's fertile period. College women sniffed and rated the attractiveness of the scent of 41 T-shirts worn over a period of two nights by different men. Results indicated that normally cycling (non-pill using) women near the peak fertility of their cycle tended to prefer the scent of shirts worn by symmetrical men. Normally ovulating women at low fertility within their cycle, and women using a contraceptive pill, showed no significant preference for either symmetrical or asymmetrical men's scent. A separate analysis revealed that, within the set of normally cycling women, individual women's preference for symmetry correlated with their probability of conception, given the actuarial value associated with the day of the cycle they reported at the time they smelled the shirts. Potential sexual selection processes and proximate mechanisms accounting for these findings are discussed.

Adolescent↗

Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi.

Sexual conflict theory predicts an antagonistic coevolution, with each sex evolving adaptations and counter-adaptations to overcome a temporary dominance of the other sex over the control of paternity. Polyandry allows sexual selection to operate after mating has commenced, with male and female interests competing for control of fertilization. There are numerous examples of male control of paternity, but few studies have unambiguously revealed female control. Attributing variance in paternity to females is often difficult since male and female influences cannot be separated unambiguously. However, we show that polyandrous female orb-web spiders Argiope keserlingi (Arancidae) control the paternity of their offspring by adjusting the timing of sexual cannibalism. Our experiments reveal that females copulating with relatively smaller males delay sexual cannibalism, thereby prolonging the duration of copulation, and that these males consequently fertilize relatively more eggs.

Animals↗

Reproductive suppression in female Damaraland mole-rats Cryptomys damarensis: dominant control or self-restraint?

Colonies of Damaraland mole-rats Cryptomys damarensis exhibit a high reproductive skew. Typically one female breeds and the others are anovulatory. Two models, the dominant control model (DCM) and the self-restraint model (SRM), have been proposed to account for this reproductive suppression. The DCM proposes that suppression is under the control of the dominant breeder and is imposed by mechanisms such as aggression, pheromones and interference with copulation, whereas the SRM does not involve aggression directed towards non-breeders and may function in order to minimize inbreeding. We investigated potential proximate mechanisms involved in the suppression of females in a series of experiments. Socially induced stress through aggression did not appear to be responsible for anovulation. Nor did breeders actively interfere with subordinate copulation. Females were physiologically suppressed when housed in intact colonies. However, as predicted by the DCM, they did not become reproductively active when removed from the presence of breeders. We found no evidence that pheromonal cues block ovulation. We suggest that the SRM is the basic model found in the Damaraland mole-rat and that self-restraint functions in order to minimize inbreeding by restricting reproduction until an unrelated male is present. This would explain the rapid onset of reproductive activation in females when paired with an unrelated male, as demonstrated in this study.

Analysis of Variance↗

Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs.

Ovarian cycles in catarrhine primates are uniquely characterized by prolonged periods of sexual activity in which the timings of ovulation and copulation do not necessarily correspond. According to current hypotheses of primate social evolution, extended sexuality in multi-male groups might represent part of a female strategy to confuse paternity in order to reduce the risk of infanticide by males. We test this hypothesis by examining mating behaviour in relation to timing of ovulation and paternity outcome in a multi-male group of free-living Hanuman langurs. Using faecal progestogen measurements, we first document that female langurs have extended receptive periods in which the timing of ovulation is highly variable. Next, we demonstrate the capacity for paternity confusion by showing that ovulation is concealed from males and that copulations progressively decline throughout the receptive phase. Finally, we demonstrate multiple paternity, and show that despite a high degree of monopolization of receptive females by the dominant male, non-dominant males father a substantial proportion of offspring. We believe that this is the first direct evidence that extended periods of sexual activity in catarrhine primates may have evolved as a female strategy to confuse paternity.

Animals↗

Parasite infection, host resistance and mate choice: battle of the genders in a simultaneous hermaphrodite.

Parasites have been proposed to be fundamental in the evolution of mate choice because differential mating on the basis of heritable disease resistance is expected to lead to progeny with a better genome-environment match than random mating. However, direct empirical data in support of this hypothesis are often lacking, and the relative influences of current and potential infection status (i.e. resistance genotype), and of mate choice versus mate conflict, remain largely unknown. We demonstrate experimentally, using simultaneous hermaphroditic snails (Biomphalaria glabrata) artificially selected for resistance or susceptibility to Schistosoma mansoni infection, that mate choice is influenced by a combination of current and potential parasitic infection status. As predicted by game-theory models, we also found a picture of conflict and cooperation: resistant and susceptible genotypes copulated in either gender and reciprocated (i.e. switched gender) equally when faced with an uninfected partner, but, by contrast, resistant snails actively refused to copulate as females with an infected partner. Such recognition and discrimination has implications for the maintenance of sex and the evolution of recognition systems.

Animals↗

Post-copulatory sexual selection and female fitness in Scathophaga stercoraria.

Whether sexual selection increases or decreases female fitness is determined by the occurrence and relative importance of sexual-conflict processes and the ability of females to choose high-quality males. Experimentally enforced polyandry and monogamy have previously been shown to cause rapid evolution in the yellow dung fly Scathophaga stercoraria. Flies from polyandrous lines invested more in reproductive tissue, and this investment influenced paternity in sperm competition, but came at a cost to immune function. While some fitness consequences of enforced polyandry or monogamy have been examined when flies mate multiply, the consequences for female fitness when singly copulated remain unexplored. Under a good-genes scenario females from polyandrous lines should be of higher general quality and should outperform females from monogamous lines even with a single copulation. Under sexual conflict, costly adaptations will afford no advantages when females are allowed to mate only once. We investigate the lifetime reproductive success and longevity of females evolving under enforced monogamy or polyandry when mating once with males from these selection regimes. Females from polyandrous lines were found to have lower fitness than their monogamous counterparts when mating once. They died earlier and produced significantly fewer eggs and offspring. These results suggest that sexual conflict probably drove evolution under enforced polyandry as female fitness did not increase overall as expected with purely good-genes effects.

Animals↗

Male red-winged blackbirds distrust unreliable and sexually attractive neighbours.

In many species, territorial neighbours fight to establish their mutual border and then develop a truce, known as the dear-enemy phenomenon, characterized by reduced vigilance and aggression along the border. We present evidence that among male red-winged blackbirds (Agelaius phoeniceus) the dear-enemy relationship is a form of reciprocal conditional cooperation that is stabilized, at least in part, by retaliation against cheaters. Simulated intrusions by randomly chosen neighbours were punished by a targeted increase in vigilance and aggression that persists for days. We interpret this increase in vigilance towards trespassers as a manifestation of distrust. The conditional decrease in vigilance and aggression is tempered by each neighbour's probability of cuckolding the focal male. Male red-winged blackbirds maintained greater vigilance and aggression towards sexually attractive neighbours that were more successful at extra-pair fertilizations (EPFs). It is unlikely that males directly observed neighbours copulating with their mates. They were more likely to assess a neighbour's ability to achieve extra-pair copulations using surrogate cues that correlate with success at EPFs, including body size. Our results suggest that red-winged blackbirds use rules that incorporate their neighbour's behaviour and quality in their territorial interactions with one another. Our results expand our understanding of cooperation for animals and for humans as well.

Aggression↗

Testosterone, cuckoldry risk and extra-pair opportunities in the Seychelles warbler.

In male birds, testosterone (T) plays an important role in aggressive and mate-attraction behaviour. In the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis, extra-group copulations (EGCs) occur frequently, but are not accompanied by sexual courtship displays as in within-pair copulations. Paternity is nearly always gained by primary males. We investigated whether T levels and sperm storage capability (cloacal protuberance (CP)) in adult primary and subordinate males were related to timing of egg laying, levels of cuckoldry and extra-group paternity (EGP) opportunities. During the sexually active period before egg laying, T levels and CP were only elevated or enlarged (respectively) in primary males, and some suggestion was found that subordinate males do not invest in elevated T levels. The peak in T occurred during the fertile period of the female partner and corresponded to the peak period of male sexual displays and mate guarding, but was independent of cuckoldry risk (density of neighbouring primary males). CP was also enhanced during this period; however, CP but not T remained elevated after egg laying by their mates, and CP but not T was positively related to EGP opportunities (density of neighbouring fertile females). We conclude that T is involved in sexual courtship displays and mate guarding, but not in gaining EGCs. These findings contrast with those in other species where EGP involves elaborate sexual displays.

Age Factors↗

Multiple sperm storage organs facilitate female control of paternity.

It has been proposed that multiple sperm storage organs (spermathecae) could allow polyandrous females to control paternity. There is little conclusive evidence for this since insemination of individual spermathecae is generally not experimentally manipulable. Here, we examined sperm use patterns in the Australian redback spider (Latrodectus hasselti), which has paired, independent spermathecae. We assessed paternity when two rivals were forced to inseminate a single storage organ or opposite storage organs. When males inseminated a single spermatheca, mean paternity of the female's first mate was 79.8% (median 89.4%), and 38% of first mates achieved 100% paternity. In contrast, when males inseminated opposite organs, the mean paternity of the first mate was 49.3% (median 49.9%), only 10% of males achieved complete precedence, and paternity was normally distributed, suggesting sperm mixing. Males responded to this difference by avoiding previously inseminated female reproductive tracts. Complete sperm precedence can only be achieved if females permit males to copulate with both reproductive tracts. Females often cannibalize smaller males during their first copulation, thus limiting their paternity to 50%. These data show that multiple sperm storage organs can increase female control of paternity.

Animals↗

Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants.

The reproductive interests of males and females are not always aligned, leading to sexual conflict over parental investment, rate of reproduction and mate choice. Traits that increase the genetic interests of one sex often occur at the expense of the other, selecting for counter-adaptations leading to antagonistic coevolution. Reproductive conflict is not limited to intraspecific interactions; interspecific hybridization can produce pronounced sexual conflict between males and females of different species, but it is unclear whether such conflict can drive sexually antagonistic coevolution between reproductively isolated genomes. We tested for hybridization-driven sexually antagonistic adaptations in queens and males of the socially hybridogenetic 'J' lineages of Pogonomyrmex harvester ants, whose mating system promotes hybridization in queens but selects against it in males. We conducted no-choice mating assays to compare patterns of mating behaviour and sperm transfer between inter- and intra-lineage pairings. There was no evidence for mate discrimination on the basis of pair type, and the total quantity of sperm transferred did not differ between intra- and inter-lineage pairs; however, further dissection of the sperm transfer process into distinct mechanistic components revealed significant, and opposing, cryptic manipulation of copulatory investment by both sexes. Males of both lineages increased their rate of sperm transfer to high-fitness intra-lineage mates, with a stronger response in the rarer lineage for whom mating mistakes are the most likely. By contrast, the total duration of copulation for intra-lineage mating pairs was significantly shorter than for inter-lineage crosses, suggesting that queens respond to prevent excessive sperm loading by prematurely terminating copulation. These findings demonstrate that sexual conflict can lead to antagonistic coevolution in both intra-genomic and inter-genomic contexts. Indeed, the resolution of sexual conflict may be a key determinant of the long-term evolutionary potential of host-dependent reproductive strategies, counteracting the inherent instabilities arising from such systems.

Animals↗

Mutual interest between the sexes and reproductive success in Drosophila pseudoobscura.

The pre-mating behavior of female Drosophila pseudoobscura has been considered passive and "coy" relative to more active, "ardent," and indiscriminate male behavior. To test whether this long-held view-the "received wisdom" about mating behavior in Drosophila-is really true we carried out observations on how often D. pseudoobscura females approached males prior to courtship and copulation. By including only virgin females and males in the experiments, we eliminated the possibility that males are "coy" due to sperm limitation and females flexibly "coy" due to male manipulations that may affect the duration of remating inhibition. We observed the movements of females and males in vials during the first five minutes of exposure to one another. Video records revealed females went toward males as frequently as males toward females; we inferred that females were as interested in males as males in females. The total number of offspring emerging as adults correlated significantly with mutual, precourtship interest of both males and females in their vial-mates and latency to copulation. Thus, we hypothesize that females in nature approach males, perhaps actively soliciting male courtship simply by remaining close to them.

Animals↗