Single Copulation Research Articles

Do femaleDrosophila melanogasteradaptively bias offspring sex ratios in relation to the age of their mate?

Modification of offspring sex ratios in response to parental quality is predicted when the long-term fitness returns of sons and daughters differ. One factor that may influence a mother's sex allocation decision is the quality (or attractiveness) of her mate. We investigated whether the sex ratios of offspring produced by female Drosophila melanogaster are biased with respect to the age of the males to which they are mated, and whether there is an adaptive basis for this phenomenon. We found that females mated to old males (13 d post-eclosion) initially produced a greater proportion of daughters than did females mated to young males (1 d post-eclosion). This pattern does not appear to be due to a systematic difference in the numbers or mortality of the X- and Y-bearing sperm originating from old and young fathers, as the overall sex ratios of all offspring produced from a single copulation did not differ between broods fathered by the two types of males. The sons of older males fared worse in competitive mating assays than did the sons of younger males, while daughters of old and young males were of comparable fitness. These results suggest that there is an adaptive basis for the observed sex ratio modification.

Estimation of relative reproductive expenditure in the courtship-role-reversed bean weevil, Bruchidius dorsalis (Fahraeus)

It is often difficult to measure the parental expenditure on reproduction by both sexes, because even in species where both sexes invest only nutrient to produce eggs, the nutrition invested by the male is inevitably mixed with that from the female in the body of the female. In this paper, I propose a regression-analysis-based method to estimate the relative amount of investment by both sexes separately, which I have applied to the bean weevil Bruchidius dorsalis (Fahraeus: Bruchidae; Coleoptera), which shows role-reversal in its courtship behavior. The results indicated that lifetime maternal expenditure (the estimated intercept) was fivefold higher than paternal expenditure in a single copulation (the estimated coefficient). Although the number of copulations by wild males was not measured in this study, it is unlikely that they copulate fewer than six times during their lifetime, judging from their longevity and the frequency of copulation in the laboratory. In the experiment, males were divided into two different feeding regimes to test whether their nutritional condition affected their paternal expenditure, but no significant effect was detected.

Dynamics of eupyrene and apyrene sperm storage in ovipositing females of the swallowtail butterfly Papilio xuthus (Lepidoptera: Papilionidae)

AbstractA male swallowtail butterfly, Papilio xuthus, transfers both eupyrene and apyrene sperm during copulation, both of which migrate to the spermatheca via the spermatophore in the bursa copulatrix of the female. Because the spermatheca seems to remain constant in size during the female lifespan, the excess sperm migration may cause the spermatheca to overflow. Approximately 9000 eupyrene and 265 000 apyrene spermatozoa were transferred during a single copulation, and approximately 1000 eupyrene and 1100 apyrene spermatozoa successfully arrived in the spermatheca. The number of both types of spermatozoon decreased in the spermatheca after the onset of oviposition, and no eupyrene spermatozoa were found by 7 days after copulation, partly due to insemination. The spermathecal gland leading from the distal end of the spermatheca was gradually filled by eupyrene spermatozoa. Although the function of the gland remains unclear, the final destination of the sperm is likely to be the gland.

Sperm storage and use in laboratory-reared Aplysia californica , a simultaneous hermaphrodite

Aplysia californica, an opisthobranch mollusc, possesses a complex reproductive system that includes a seminal receptacle for the storage of exogenous sperm received from mating. Based on this reproductive anatomy, A. californica should have the ability to maintain and use viable exogenous sperm stores to fertilize multiple eggmasses for extended periods of time. Using controlled matings and careful observation of the development of eggmasses over time, we attempted to quantify A. californica’s ability to store and use exogenous sperm following a single mating. On average, A. californica (240.6±31.7 g; mean±SE, n=9) produced 8.8±0.6 eggmasses containing 16.9±2.2×106 fertilized eggs over a period of 22.3±3.6 days following a single mating encounter. The maximum duration an individual A. californica produced fertilized eggs, following a single copulation, was 41 days. The primary factor determining the cumulative number of fertilized eggs produced from a single mating in A. californica was the mass of the sperm recipient (r=0.773, P<0.05, n=9). Our results demonstrated that A. californica are not sperm limited following a single mating as has been suggested for other opisthobranch molluscs by Leonard and Lukowiak’s (1991) gamete-trading hypothesis.

Social Monogamy in the Big‐Clawed Snapping Shrimp, Alpheus heterochelis

AbstractSocial monogamy has evolved independently in many taxa, and often involves biparental care of the young. Where it does not, mate guarding and shared territoriality have been invoked as causal factors. We evaluated mate guarding and shared resource defence (a common shelter) as factors that could have led to social monogamy in the snapping shrimp, Alpheus heterochelis. This species is found in male–female pairs that defend a common shelter together. Female receptivity lasts only for a few hours immediately after her periodic moult. Their monogamous pair bond may represent mate guarding or joint defence of a territory. Monogamy in A. heterochelis seems most importantly driven by the cryptic nature of the female's moult cycle. We found that males did not discriminate among females at different intermoult stages for pairing, nor did they modulate their defence of mate and shelter (vs. the risk in finding a new shelter and mate) according to female moult stage. This, together with the short period of female receptivity before her single copulation per cycle, make extended mate guarding the most efficient method for a male to secure a mating opportunity. Comparing eviction rates of paired and unpaired shelter residents by conspecific intruders provided no evidence of enhanced resource defence that would confer a selective advantage to a pair. Male presence during the moult is beneficial for the female, as searching for a male during her soft‐bodied receptive phase would put her at mortal risk. Our results show empirically for the first time that guarding may be beneficial, even if males are not able to assess the female's reproductive stage. This extends the theoretical framework for understanding the evolution of social monogamy in taxa without biparental care of young.

Tests of hypotheses on the adaptive value of an extended male phase in the hermaphroditic shrimp Lysmata wurdemanni (Caridea: Hippolytidae).

Hypotheses on delayed sex change in the protandric simultaneous hermaphrodite Lysmata wurdemanni were tested with observations from population samples, mating experiments, and experiments on sex change under optimal and suboptimal breeding conditions. Male-phase individuals (MPs) much larger than the minimum size of sex change were most frequent in a natural population from fall through early spring. The hypothesis was tested that some MPs delay sex change to the simultaneous hermaphrodite female-phase (FP) because MPs are more competitive in obtaining copulations with parturial FPs than are FPs mating as males (MFPs). In different experiments, parturial FPs were maintained with two potential male mating partners (large MP and MFP, small MP and MFP, large MP and small MP) through the parturial molt and spawning; activities were recorded with time-lapse video. MFPs gained the single copulation with the parturial FP as frequently as MPs, large or small, but large MPs copulated with more FPs than small MPs. The hypothesis of FP reversion to large MP was tested experimentally and rejected. Rate of change of MP to FP was much lower in large MPs maintained under suboptimal (fall/winter) than optimal (spring/summer) breeding conditions. The results presented here suggest that the occurrence of large MPs from the fall to early spring is better explained by abiotic proximate factors related to breeding than by socially mediated sex change in different demographic environments.

The relationship between sperm reservoir and spermatophore length in benthic octopuses (Cephalopoda: Octopodidae)

The relationship between sperm reservoir and total spermatophore length among 168 spermatophores from 44 species in 11 genera has been considered. Bivariate plots show that four Atlantic species of the genus Eledone produce spermatophores with relatively large sperm reservoirs that differ from all others. Measurements of the remaining spermatophores are so tightly correlated that a single equation explains over 96% of the variation. Functional constraints on gross spermatophore morphology may be so strong that males cannot manipulate sperm reservoir size independently of spermatophore size to maximize the sperm delivered at a single copulation. Alternate means to assure male paternity may have evolved in the group as a result. Despite the overall uniformity of the relationship among all species other than those of Eledone in the Atlantic, these measurements distinguish the overtly similar species Octopus bimaculatus–Octopus bimaculoides and separate Benthoctopus januarii from all others.

Copulation and sperm release in Gasteracantha cancriformis (Araneae: Araneidae): differential male behaviour based on female mating history

Female spiders have two separate reproductive tracts, one on each side of the body, which receive and store sperm. Thus, females may be virgin or nonvirgin on both sides, or virgin on one side and nonvirgin on the other side. To examine whether male orb-weaving spiders, G.cancriformis, respond differentially to females based on mating history, we presented males to (1) virgin females, (2) females that had previously mated with one of their two tracts and (3) females that had mated previously with both reproductive tracts. Prior to copulation, males showed no differential responses in terms of latency to courtship, number of courtship bouts, number of insertion attempts, or latency to copulation. Female mating history influenced copulatory frequency and sperm release by the male, but not duration of copulation. Nearly all males copulated twice with virgin females, once with each reproductive tract. They released nearly all sperm contained in their palps. Males that encountered nonvirgin reproductive tracts were more likely to depart after a single copulation without attempting a second. Such males rarely released sperm, but the few that did released as many as males mating with virgin tracts. Thus, sperm were released in an all-or-none fashion. Female mating history did not influence the frequency of intersexual cannibalism. This suggests that differential response by males is more likely related to female patterns of sperm use than to high levels of intersexual killing.

Selection of male traits during and after copulation in the seedbug Lygaeus simulans (Heteroptera, Lygaeidae)

In order to evaluate selection of male morphological traits during copulation, a laboratory experiment was performed with the promiscuous seedbug Lygaeus simulans. Three male traits suspected as putative targets of selection were measured: weight, fluctuating asymmetry of a measure on the forewings, and length of a conspicuous genital structure, the processus gonopori. As fitness measures we considered total fecundity (number of fertilized eggs), insemination and fertilization success (established if a female laid fertilized eggs after copulation), and the interval between copulation and oviposition. Eighty-four males were allowed a single copulation with one virgin female each. Out of 67 copulations, 27 (40.2%) resulted in fertilized eggs and the oviposition latency ranged from 6 to 26 days. Regressions of male traits on the fitness measures showed significant phenotypical selection of two male traits: (1) males of average weight are more likely to achieve fertilization and (2) the oviposition latency was shorter for males with lower asymmetry. The copulation–oviposition interval may be especially important for male fertilization success because Lygaeus males perform copulatory mate guarding and the last male copulating with a female fertilizes most of the eggs. No selection of the genitalic trait was detected.

Selection of male traits during and after copulation in the seedbug Lygaeus simulans (Heteroptera, Lygaeidae)

Abstract In order to evaluate selection of male morphological traits during copulation, a laboratory experiment was performed with the promiscuous seedbug Lygaeus simulans . Three male traits suspected as putative targets of selection were measured: weight, fluctuating asymmetry of a measure on the forewings, and length of a conspicuous genital structure, the processus gonopori. As fitness measures we considered total fecundity (number of fertilized eggs), insemination and fertilization success (established if a female laid fertilized eggs after copulation), and the interval between copulation and oviposition. Eighty-four males were allowed a single copulation with one virgin female each. Out of 67 copulations, 27 (40.2%) resulted in fertilized eggs and the oviposition latency ranged from 6 to 26 days. Regressions of male traits on the fitness measures showed significant phenotypical selection of two male traits: (1) males of average weight are more likely to achieve fertilization and (2) the oviposition latency was shorter for males with lower asymmetry. The copulation–oviposition interval may be especially important for male fertilization success because Lygaeus males perform copulatory mate guarding and the last male copulating with a female fertilizes most of the eggs. No selection of the genitalic trait was detected.

Insemination efficiency of two alternative male mating tactics in the guppyPoecilia reticulata

In this study we compared the insemination efficiency of two alternative mating tactics (courtship and sneak mating) in the guppy Poecilia reticulata by quantifying the number of sperm delivered during a copulation. During a single copulation, guppies delivered between zero and 92% of the sperm available, as determined by mechanically stripping the male's sperm reserve at rest. The absolute number of sperm delivered after courtship was three times larger than that delivered through sneak mating; nonetheless, the variance was large with both tactics and the two distributions largely overlapped. The number of sperm available at rest increased with male size. With both tactics, the number of sperm delivered was positively correlated with the sperm available. Contrary to courtship copulations, in sneak copulations there was no correlation between the number of sperm delivered and male size. However, once the data were standardized for sperm reserve, small males delivered a larger proportion of their available sperm during sneak copulation. The rate of sexual acts (sigmoid and thrust rate) before copulation was not correlated with the number of sperm available. After the occurrence of a copulation in both the courtship and sneak copulation groups, the sexual activity of the male decreased in proportion to the amount of sperm he previously inseminated.

The beneficial sexually transmitted microbe hypothesis of avian copulation

Several hypotheses have been proposed to explain why female birds either copulate repeatedly with a single mate or copulate with multiple partners even though only a single copulation may be sufficient to fertilize an entire clutch. We hypothesize that females may directly benefit from high frequencies of copulation and multiple copulation partners if they receive a cloacal inoculation of beneficial sexually transmitted microbes (STMs) that can either protect them against future encounters with pathogens and/or serve as therapy against present infections. Experiments in domestic animal production, wildlife rehabilitation, and clinical medicine indicate that inoculations of beneficial microbes derived from the indigenous microflora of hosts can lead to nutritional benefits, resistance to colonization by pathogens, the elimination of infection, and improved immune system functioning in recipients. Our hypothesis predicts greater copulatory rates when the probability of the transmission of beneficial microbes exceeds that of pathogens and when the positive effects of beneficial microbes on host fitness exceed the negative effects of pathogens. Patterns of copulatory behavior in birds suggest the potential utility of our hypothesis. We discuss our hypothesis in the context of observed patterns of copulation in birds and propose some ways to directly test our hypothesis. Information on the probabilities of transmission during copulation of beneficial and pathogenic microbes and their relative potencies in birds are needed to directly test the predictions of our hypothesis.

Costs and benefits for water strider (Aquarius paludum) females of carrying guarding, reproductive males

We describe the mating system of Aquarius paludum insularis based on field observations and test hypotheses about the effects of body size, hunger level and post‐copulatory guarding on reproductive performance. The mating sequence of this species was typical for temperate water striders, except that most oviposition was carried out by tandem pairs, most of which were submerged. Mate guarding continued until the end of oviposition, lasting up to 18.2 h, which was much longer than that recorded for other species of water striders. Pair partners changed after oviposition. Extended contact guarding reduced female mobility. In the case of females that carried long‐winged males, there was a significant reduction in speed and stride between tandem as opposed to single females. However, when short‐winged males were carried, there was not a significant difference. Short‐term foraging efficiency did not differ significantly between tandem and single females, and thus did not reflect the difference in mobility. Hunger level did not significantly affect female mating receptivity. Although the number of harassment bouts by unpaired males did not differ between single and tandem females, single females suffered significantly more harassment. Females were able to lay fertilized eggs for about 15 days after a single copulation, but they accepted long guarding and multiple mating during this period as well. The cost of resisting male mating attempts appears to be greater than the cost of carrying males.

Relationship between aging, mating and sperm production in captive Bombus terrestris

SUMMARYMating behaviour of Bombus terrestris, its sperm production and sperm transfer to queens were studied in parallel, under controlled conditions. The mean value of the age of mating was 6.1 days (s.e. = 0.4 days) for queens and 12.1 days (s.e. = 1.3 days) for males. The average sperm content of vasa deferentia ranged between 4000 and 230 000 spermatozoa per male. It increased from emergence up to the sixth day. The age at which males mated extended from the sixth day to day 27. Chances to cause queens to mate dropped dramatically after day 11. Spermatheca contents varied from 5800 to 36 200 spermatozoa after a single copulation with virgin males. The efficiency of mating in terms of sperm transfer to spermatheca was not affected by the age but was reduced by previous copulations of the male.

Transport of spermatozoa and ova in female alpaca

Transport of spermatozoa and ova were studied in female alpaca. Fifteen parous females were slaughtered at 6 h, 12 h, 18 h, 24 h and 30 h after a single copulation to determine the time taken for spermatozoa to reach the oviduct. Twelve parous females were slaughtered at 4 days, 7 days and 10 days after copulation to determine when the ovum reached the uterus. Spermatozoa and ova were collected by flushing portions of the oviduct and uterus. Spermatozoa were present at the site of fertilization 6 h after copulation and remained there for up to 30 h. There was a retrograde sperm flow back to the uterus by 18 h after copulation. The utero-tubal junction was the main location where sperm were stored. Fertilized ova at the morula stage were collected from oviducts by 4 days after copulation and compacted morulae by 7 days. Blastocysts were collected from the uterine horn 10 days after copulation.

Multiple mating in the ant Acromyrmex versicolor : a case of female control

In eusocial insects, polyandrous mating has the potential to reduce genetic relatedness of individuals within a colony, which may have a profound effect on the stability and social structure of the colony. Here we present evidence that multiple mating is common in both males and females of the desert leaf-cutter ant Acromyrmex versicolor. Females seem to have complete control over the number of matings, and mate on average with three males, even though the sperm transferred in a single copulation is sufficient to fill the spermatheca. To determine whether there is a bias in the representation of sperm from different mates in the spermatheca, females were mated to three or four males in controlled mating experiments and were subsequently allowed to found colonies in the laboratory. Paternity analysis of the offspring by random amplified polymorphic DNA analysis showed that all males that have been mated to a female successfully contributed sperm to the production of her offspring. No significant asymmetry in sperm use was detected, suggesting complete sperm mixing. Different hypotheses to explain polyandrous mating are discussed, and it is argued that the best hypothesis to explain polyandrous mating and complete sperm mixing in A. versicolor is that utilizing genetically diverse sperm confers a selective advantage on females.

Dose response to equine chorionic gonadotropin and subsequent ovulation in llamas

Multiple ovarian follicles were induced to grow and ovulate in llamas by administration of equine chorionic gonadotropin (eCG) followed by either copulation or injection of human chorionic gonadotropin (hCG). Forty-five parous female llamas were divided randomly into five treatment groups: control ( n = 8), 100 ( n = 7), 500 ( n = 10), 1000 ( n = 10) or 2000 ( n = 10) IU eCG. Ultrasonography was used to monitor ovarian activity during the ovarian cycle, urinary estrone sulfate during the follicular phase, and pregnanediol during the luteal phase. The number of follicles was not different ( P > 0.05) between control and females receiving 100 IU eCG. Follicular growth was increased ( P < 0.05) seven days after treatment with doses of at least 500 IU eCG. A mean number of 4.7, 4.6, and 6.4 follicles was observed for doses of 500 IU, 1000 IU, and 2000 IU eCG, respectively. Concentrations of urinary estrone sulfate increased ( P < 0.05) three-fold in animals with multiple follicles (101 ng mg −1 creatinine (Cr)) compared with animals bearing single follicles (29.7 ng mg −1 Cr). Cystic follicles occurred in two, two, and nine animals receiving 500 IU, 1000 IU and 2000 IU eCG, respectively. Twenty females were induced to ovulate with either single copulation (11) or 750 IU hCG administration (9). Corpora lutea were observed in 59.9% and 78.8% ( P < 0.05) of females stimulated with single copulation or hCG, respectively. Mean number of corpora lutea was 3.4 and 5.4, respectively. Concentrations of pregnanediol were 9.3 and 7.7 ng mg −1 Cr, respectively, at day 7 after copulation or hCG. Although 2000 IU eCG provoked multiple follicle development, most of them became cystic. Doses of 500 and 1000 IU eCG were optimal doses for inducing multiple follicle growth in llamas, while hCG administration was superior to copulation for stimulating ovulation.

Reproductive behaviour in the female blind mole rat (Spalax ehrenbergi)

The mole rat (Spalax ehrenbergi) is a blind, solitary, highly aggressive subterranean rodent well adapted to underground life, and in Israel involves four chromosomal species (Nevo, 1991). Little is known to date about its reproductive biology and all attempts to breed mole rats in captivity have failed. The present study investigated the effects of three different light regimes on vaginal smear and annual cycle of body weight, age at sexual maturity, and various parameters of reproductive behaviour of female mole rats. Daily vaginal smears throughout the year revealed that the mole rat does not have a regular oestrous cycle, but exhibits an annual rhythm with a seasonally cornified smear. Regardless of the photoperiods the females were exposed to in the laboratory, relatively high proportions of cornified smears were found during the winter breeding season. A second, albeit small, peak of cornified cells was found during the summer season. Photoperiod had no effect on annual body mass cycle either, and mole rats kept under the different lighting regimes reached their maximum weight just prior to the beginning of the breeding season. In young females, vaginal opening occurs at the age of four weeks and first cornified smear at the age of 4–7 months. The presence of a cornified smear was found to be an insufficient criterion for receptivity, but providing the opportunity for a female to choose her mate enhances the chances of copulations occurring during encounters. We conclude that the mole rat is a seasonal breeder which reproduces during the winter, but has the potential of summer breeding too. Our findings also suggest that females probably have the potential to breed in their first winter. The seasonally constant vaginal smear periods, and the post copulation vaginal smear data are the first evidence suggesting that the mole rat is a reflex ovulator, but the ovulatory failure we observed after single copulations raises the possibility that multiple copulations are necessary to induce ovulation.

Extra-pair fertilizations and paternity defence in house martins,Delichon urbica

DNA fingerprinting showed that 15% of 62 house martin nestlings at study colonies in central Scotland were not related to their putative fathers, and 32% of 19 broods contained at least one extra-pair chick. There was no evidence of intraspecific brood parasitism. Birds were never seen to mate outside nests in the vicinity of nesting colonies, and the single copulation that was observed during this study was a pair mating that took place inside a nestbox. Extra-pair birds were often seen to enter nests, with seven of eight identified intruders being males from other nests where laying had already taken place. Pair males mate guarded by ensuring that females spent very little time alone at the nest from about 7 days before the first egg of the clutch was laid, and by accompanying females on up to 70% of flights away from the nest during the 4-5 days before laying commenced. Mate guarding seemed to slacken after egg laying began, with a gradual transition to incubation behaviour taking place. Associated with this was a higher likelihood that the youngest nestling would be fathered by an extra-pair male. Male removal experiments indicated that extra-pair birds were more likely to enter the nest of a fertile female when the pair male was absent, but in three cases where DNA fingerprints were obtained male removal during the fertile period of the pair female had no apparent influence on paternity.

Social and Genetic Aspects of Paternity in Wild Long-Tailed Macaques (Macaca Fascicularis)

AbstractIn a field study of three groups of wild long-tailed macaques, Macaca fascicularis, observations on social behaviour could be related to genetically determined paternity. In contrast to what has been found in many previous studies on captive primate groups, we found a relatively strong correlation between male dominance rank and reproductive success. In a large group the high success of the alpha male compared to other males could be explained only partly by his higher copulation score. His success also resulted partly from better timing of his copulations during maximum fertility of the females, in comparison with other males. We must conclude either that the alpha-male has more access to fertile females, or that females have a preference for the alpha-male during their maximum fertility. The females clearly displayed promiscuous behaviour. This behaviour implies a risk to a female that a male other than the alpha-male with proven qualities will become the father of her offspring. One expects that there must be a social advantage related to this female strategy. In the absence of indications of any direct social advantages to the female of this sexual behaviour pattern, the ultimate explanation for this female promiscuity is most likely is aggression reduction. This could be either through the devaluating of any single copulation, or through the confusion of paternity and a resultant reduction in the risk of infanticide.