The evolution of female copulation calls in primates: a review and a new model

Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.     

Do the size and age of mating plugs alter their efficacy in protecting paternity?

An obvious means to secure paternity is the production of a mating plug that blocks the female genital opening after mating. Although the mechanical efficacy and persistence of plugs on/in the female genital openings are key traits that determine the degree of paternity protection, these factors have hardly been explored. We therefore investigated the influence of the size of the amorphous plug material (experimentally terminated mating duration as a proxy) and age of the mating plug (time interval between copulations with two successive males) on the efficacy of the plug by analysing the mating success of subsequent males in the dwarf spider Oedothorax retusus (Linyphiidae: Erigoninae). Overall, subsequent males attempted to mate in 82 % of trials but only 32.5 % of these resulted in copulation, demonstrating that the plugs are effective safeguards against remating. Remating probability was significantly higher after previous short copulations (~small plug size) compared to long copulations (~large plug size). In the small plug group, fresh plugs (short remating intervals) were significantly less effective compared to older plugs. In the large plug group, remating probability was similarly low over all remating intervals. The observed copulations, however, do not necessarily result in sperm transfer, since sperm masses were found on the plugged female genital area. Our study on O. retusus shows that mating plugs are a powerful mechanical safeguard whose efficacy varies with plug size and age. We discuss these findings in the light of theoretical considerations on the evolution of effective mating plugs.     

Mate choice in the face of both inbreeding and outbreeding depression in the intertidal copepod Tigriopus californicus

 In species vulnerable to both inbreeding and outbreeding depression, individuals might be expected to choose mates at intermediate levels of genetic relatedness. Previous work on the intertidal copepod Tigriopus californicus has repeatedly shown that crosses between populations result in either no effect or hybrid vigor in the first generation, and hybrid breakdown in the second generation. Previous work also shows that mating between full siblings results in inbreeding depression. The present study again found inbreeding depression, with full sibling mating causing significant fitness declines in two of the three populations assayed. In the mate choice assays, a single female was combined with two males. Despite the costs of both inbreeding and outbreeding, mate choice showed clear inbreeding avoidance but no clear pattern of outbreeding avoidance. This lack of outbreeding avoidance may be attributed either to the temporary increase in fitness in the F₁ generation or to the absence of selection for premating isolation in wholly allopatric populations with infrequent migration. If this inability to avoid unwise matings is common to other taxa, it may contribute to the problem of outbreeding depression when allopatric populations are mixed together. Received: 18 May 1999 / Accepted: 25 January 2000     

Determinants of paternity success in the spider Pholcus phalangioides (Pholcidae: Araneae): the role of male and female mating behaviour

In double mating experiments, we examined whether and to what extent various male and female behavioural traits influence the course of mating and fertilization success in the cellar spider. In males, we focussed on pre-copulatory behaviour and on the rhythmic twisting movements that the male performs with his pedipalps during copulation. In females, we investigated remating decisions and the effect of female termination of copulation. Second males fertilized a high proportion of the eggs (P ₂: median 89%) despite much shorter second matings, with high variation in relative paternity success. The number of pedipalp movements (PPMs) of either male was a better predictor of paternity than copulation duration. Our results suggest that in second matings, PPMs help to remove sperm from previous males, whereas in first matings a high number of PPMs enhances fertilization success, either due to numerical sperm competition or cryptic female choice. Furthermore, we found a negative male age effect on paternity in second matings, implying that age-related deterioration of spermatozoa may promote variation in fertilization success. Female receptivity decreased significantly in second matings; only 70% of the females remated. Females that accepted a second copulation were found to terminate these much earlier and with higher probability than first matings. This suggests that the intensity of conflict between the sexes is higher in second matings. Increased intensity of sexual conflict may be responsible for stronger selection on male traits, as pre-copulatory behaviour and age only affected male copulatory performance and paternity in second matings. Electronic Publication     

Copulation duration and sperm competition in white-faced dragonflies (Leucorrhinia intacta; Odonata: Libellulidae)

Summary In many odonates, females mate with more than one male while laying a single clutch of eggs. We studied paternity of eggs laid by remated females of Leucorrhinia intacta, a small libellulid dragonfly, at a pond near Syracuse, NY, USA. The probability of a female remating is a function of male density on the pond. The length of copulations differs considerably among males active on the study pond at the same time. Much of this variation was correlated with differences in mating tactics of the males; copulations by males that stayed on their territories during copulation were shorter than those by other males (Fig. 2). Eggs collected from females mated to irradiated, sterile males and to free-living, fertile males indicated that the average paternity expectation was higher for long than for short copulations, and that the variance in paternity expectation was lower for long than for short copulations. Some possible causes of the high variation in paternity at low copulation durations and possible reasons for differences in copulation duration between male mating tactics are discussed.     

Mating with a kin decreases female remating interval: a possible example of inbreeding avoidance

Inbreeding depression is a relative decline in fitness in offspring of related parents. The magnitude of inbreeding costs varies among taxa and may increase under stressful conditions. Inbreeding tolerance is expected to be low and selection for inbreeding avoidance intense when both sexes invest substantially in shared offspring like in nuptial gift-giving butterflies. This is especially true for increasing mating rate for inbreeding avoidance as nuptial feeding decreases net costs of mating for females. We explored implications of inbreeding in the nuptial gift-giving green-veined white butterfly, Pieris napi. Compared to outbred ones, partially inbred (F = 0.25) eggs and neonate larvae had 25% lower hatching success and 30% lower survival until adult eclosion, respectively. Inbreeding was also associated with small size. Yet, the magnitude of inbreeding depression was independent of larval conditions. A lack of assortative mating and mating durations independent of mating type suggest that neither females nor males discriminate close relatives (r = 0.5) as mates. Indicative of a postcopulatory mechanism to avoid inbreeding, female remating intervals decreased following incestuous matings. Such a plastic response may affect the level of postcopulatory sexual selection as female remating interval (time between successive matings) is necessarily negatively correlated with mating rate (matings per unit time) and mating frequency (lifetime number of matings), and precopulatory mate choice appeared insignificant. Moreover, incest-induced shift in the phenotype towards the adaptive peak may contribute to the evolution of female mating rates, although alternative explanations for polyandry besides material benefits have rarely been invoked when nuptial feeding is involved.     

Why do female mice mate with multiple males?

Females often show multi-male mating (MMM), but the adaptive functions are unclear. We tested whether female house mice (Mus musculus musculus) show MMM when they can choose their mates without male coercion. We released 32 females into separate enclosures where they could choose to mate with two neighboring males that were restricted to their own territories. We also tested whether females increase MMM when the available males appeared unable to exclude intruders from their territories. To manipulate territorial intrusion, we introduced scent-marked tiles from the neighboring males into males' territories, or we rearranged tiles within males' own territories as a control. Each female was tested in treatment and control conditions and we conducted paternity analyses on the 57 litters produced. We found that 46 % of litters were multiply sired, indicating that multiple paternity is common when females can choose their mates. Intrusion did not increase multiple paternity, though multiple paternity was significantly greater in the first trial when the males were virgins compared to the second trial. Since virgin male mice are highly infanticidal, this finding is consistent with the infanticide avoidance hypothesis. We also found that multiple paternity was higher when competing males showed small differences in their amount of scent marking, suggesting that females reduce MMM when they can detect differences in males' quality. Finally, multiple paternity was associated with increased litter size but only in the intrusion treatment, which suggests that the effect of multiple paternity on offspring number is dependent on male–male interactions.     

The effects of male and female genotype on variance in male fertilization success in the red flour beetle (<Emphasis Type="Italic">Tribolium castaneum</Emphasis>)

The number of eggs fertilized by a male at any given copulation (fertilization success) is affected by a large number of factors. Male insemination and sperm competition success and various female structures and/or processes that bias paternity in favor of some males over others (cryptic female choice) are all likely to affect fertilization success. We suggest that more comprehensive measures of male fertilization success can increase our understanding of postcopulatory sexual selection. To improve our understanding of the importance of various sources of variance in male fertilization success, we conducted a series of experiments using flour beetles. Different wild-type strains were used in reciprocal double mating experiments, against a phenotypic marker strain. We assessed the relative effects of female genotype, male genotype and mating order on independent and inclusive measures of male defense ability ( P ₁), male offense ability ( P ₂), and female remating behavior. Female genotype influenced both P ₁ and P ₂, and male genotype interacted strongly with female genotype in its effect on P ₂. We also documented an interaction between female and male genotypes in the effects of mating on female remating behavior, such that females tended to remate most rapidly when mated to males of their own genotype. It is clear from our experiments that cryptic female choice influences the pattern of fertilization success in flour beetles, and we suggest that cryptic female choice may often be an important component of postcopulatory sexual selection. Future investigations would benefit from studying the multiple components of variance in male fertilization success.     

Why do male Callosobruchus maculatus beetles inseminate so many sperm?

Male Callosobruchus maculatus F. (Coleoptera: Bruchidae) inseminate more sperm than females can effectively store in their spermathecae. This study examines the adaptive significance of excess sperm transfer by measuring components of male and female reproductive success in response to manipulating the number of sperm inseminated. The number of sperm transferred during copulation was reduced from 56,000 ±4,462 to 8,700±1,194 by sequentially mating males to virgin females. Reducing the number of sperm inseminated by the first male to mate had no effect on the extent of sperm precedence, but reducing the number of sperm inseminated by the second male resulted in a significant reduction in the extent of sperm precedence. When large numbers of sperm are inseminated the remating refractory period of females is increased. These results indicate that males transferring large numbers of sperm during copulation have a two-fold advantage at fertilization; they are more effective at preempting previously stored sperm and they are likely to father more offspring by delaying the time of female remating. The transfer of excess sperm does not appear to serve as nonpromiscuous male mating effort; the number of eggs laid, their fertility and the subsequent survival of zygotes were unaffected by manipulating the number of sperm inseminated. The underlying mechanisms of sperm precedence were also examined. Simple models of sperm displacement failed to accurately predict the patterns of sperm precedence observed in this species. However, the results do not provide conclusive evidence against the models but rather serve to highlight our limited understanding of the movement of sperm within the female's reproductive tract.     

Inbreeding and local mate competition in the ant Cardiocondyla batesii

The ant species Cardiocondyla batesii is unique in that, in contrast to all other ant species, both sexes are flightless. Female sexuals and wingless, ergatoid males mate in the nest in autumn and young queens disperse on foot to found their own colonies in spring. The close genetic relatedness between queens and their mates (r_qm=0.76±SE 0.12) and the high inbreeding coefficient (F=0.55; 95%CI 0.45–0.65) suggest that 83% of all matings are between brothers and sisters. As expected from local mate competition theory, sex ratios were extremely female biased, with more than 85% of all sexuals produced being young queens. Despite the common occurrence of inbreeding, we could not detect any adult diploid males. Though the probability of not detecting multiple mating was relatively high, at least one-third of all queens in our sample had mated more than once. Multiple mating to some extent counteracts the effects of inbreeding on worker relatedness (r_ww=0.68±SE 0.05) and would also be beneficial through decreasing diploid male load, if sex was determined by a single locus complementary system.Communicated by L. Sundström     

Dimethyl disulfide and dimethyl trisulfide: so similar yet so different in evoking biological responses in saprophilous flies

Dimethyl disulfide (DMDS) and dimethyl trisulfide (DMTS) are used by saprophilous insects to locate breeding sites (decaying organic matter), and by brood-site deceptive flowers to attract such insects. However, little is known about the relative importance of these two compounds in eliciting electrophysiological and behavioral responses in the insects. Here, we compared the relative attractiveness of DMDS and DMTS to saprophilous flies in field choice experiments and tested whether potential differences in field responses can be explained by differences in electrophysiological antennal responses to these compounds. Field experiments revealed that the attractiveness of a mixture of these compounds is due to DMTS alone. This result was confirmed by electroantennographic recordings in which flies of four tested species of Calliphoridae (Lucilia sericata, L. caesar, Calliphora vicina, Protocalliphora azurea) and one Muscidae (Musca domestica) respond clearly to DMTS, but not to DMDS. In house flies, however, DMTS elicited electrophysiological responses only, not reflected in behavioral assays. Despite the fact that DMTS and DMDS exhibit similar chemical structures, both the electroantennographic and field responses from saprophilous flies to these two compounds strongly differed. Our study suggests that oligosulfide-responsive saprophilous flies rely on DMTS and not DMDS for finding appropriate breeding sites and that DMTS and not DMDS could act as a key mediator for pollinator attraction in brood-site deceptive plants.     

Sperm precedence, mating interval, and a novel mechanism of paternity bias in a beetle (Tenebrio molitor L.)

When females mate with more than one male, the ensuing sperm competition leads to the evolution of male mechanisms that skew paternity. Males of the yellow mealworm beetle (Tenebrio molitor) transfer a spermatophore to females during copulation, but sperm release and storage occur later. We investigated how the interval between two matings with different males affects sperm precedence by varying the interval between the copulations so that the second mating was either: (1) before sperm release from the first spermatophore (<5 min); (2) after sperm release but before spermatophore ejection (15–20 min); (3) after spermatophore ejection but before sperm storage (4 h), or (4) after complete sperm storage (24 h). We collected offspring over a period of 2 weeks and determined paternity by protein electrophoresis. There was second-male sperm precedence in all treatments, but when the interval was <5 min, the second male usually (86% of cases) had complete sperm precedence (i.e., P ₂=1). Investigations into the mechanism of second-male sperm precedence during <5-min mating intervals indicate that sperm release from the first spermatophore is inhibited, a phenomenon which has not been previously documented. Received: 31 January 2000 / Revised: 9 June 2000 / Accepted: 26 August 2000     

Underwater oviposition in a damselfly (Odonata: Coenagrionidae) favors male vigilance,and multiple mating by females

Summary Female Enallagma hageni oviposit underwater where they are inaccessible to males. I demonstrate that males guard submerged females rather than perch sites, and are behaviorally distinct from lone males at the water. In contrast to lone males, which always attempt to copulate with females presented to them, guarding males exhibit a conditional latency to remating which corresponds closely to the time required by females to oviposit a complete clutch of eggs. By ovipositing underwater, females decrease the risk that their eggs become exposed. Risks associated with submerged oviposition favor both mate guarding, and multiple, within-clutch matings by females. Both guarding mates and lone males rescue females that float on the water surface as the result of improper resurfacing. Such behavior reduces the mortality risk to females from 0.06 to 0.02 per oviposition bout. By remating between bouts, females benefit from the additional vigilance of lone males, who rescue floating females 1.4 times as often as original mates. A second consequence of multiple mating is an increase in the selective advantage of vigilance by mates. Because receptive females become scarce by early afternoon, whereas male density remains high, a male has little (3%) chance of encountering a second receptive female that day. However, he incurs a 42% risk of losing fertilizations if he abandons a mate. For male E. hageni mate guarding functions in the context of both natural and sexual selection. It insures that a mate lives to lay a complete egg clutch in addition to protecting a male's sperm investment.     

Inbreeding avoidance or tolerance? Comparison of mating behavior between mass-reared and wild strains of the sweet potato weevil

Inadvertent selection is an important genetic process that frequently occurs during laboratory culture. The mass-reared strain of the sweet potato weevil Cylas formicarius exhibits stronger inbreeding depression than the wild strain does. When inbreeding depression occurs in a population, mating with a close relative is often considered maladaptive; however, in some contexts, the inclusive fitness benefits of inbreeding may outweigh the costs, favoring individuals that tolerate a low level of inbreeding depression. Theory predicts that mass-reared strain weevils will avoid inbreeding while wild strain weevils will tolerate inbreeding. To examine this prediction, we compared the effect of relatedness on the mating and insemination successes in mass-reared and wild strains of C. formicarius. While close relative pairs of the wild strain copulated less frequently than non-kin pairs, almost all mass-reared strain pairs copulated irrespective of relatedness. The results showed that the strain with weak inbreeding depression (wild strain) avoided inbreeding, whereas the strain with strong inbreeding depression (mass-reared strain) tolerated inbreeding. The contradiction between the theoretical prediction and our results is discussed from the perspective of laboratory adaptation, mating systems, and life history of C. formicarius.     

Female benefit,male risk: Polyandry in the true armyworm Pseudaletia unipuncta

In Lepidoptera polyandry is common and females may increase their lifetime reproductive output through repeated matings if they acquire essential resources from male ejaculates. However, the paternity of males mating with previously-mated females is far from assured unless sperm precedence is absolute. In this study on the polyandrous armyworm, Pseudaletia unipuncta, we used two strains of male (the black-eyed wild type and a red-eyed homozygous, recessive mutant), mated with red-eyed females, to determine (i) whether male investment has any impact on female reproductive output, and (ii) if females do benefit from multiple matings, to what extent males fertilize the eggs to which they contributed. Multiple mating resulted in a significant increase in both the fecundity and longevity of females. However, the degree of sperm precedence (those eggs fertilized by the second male) varied from 0–100%, but was not affected by either male size or age, or by the duration of copulation. In cases where sperm precedence was <50% (x = 12%) females produced significantly more eggs (1384 versus 940) prior to the second mating than females where sperm precedence was >50% (x = 89%), indicating that the quality of the first mating influenced the fertilization success of the female's second mate.     

Investigations of carotenoids in some fauna of the Adriatic Sea. II. Anemonia sulcata and Actinia equina (Coelenterata: Anthozoa)

Investigations have been carried out on the carotenoids in Anemonia sulcata (Pennant) and Actinia equina (L.) (Coelenterata: Anthozoa) from the Adriatic Sea. The presence of the carotenoids was determined by means of columnar and thin-layer chromatography. The following carotenoids were found: Anemonia sulcata: β-carotene, lutein-like (epoxy and free) and astaxanthin; Actinia equina: α-carotene, β-carotene, actinioerythrin, lutein-like (?) and astaxanthin (ester and free).     

Dominance rank,female reproductive synchrony,and male reproductive skew in wild Assamese macaques

In groups with multiple males, direct mate competition may select for the evolution of dominance hierarchies that sort males into a queue for access to fertile females. The priority-of-access (PoA) model proposed by Altmann in 1962 makes explicit predictions about the resulting paternity distribution based on an interaction between male dominance rank and the overlap of female receptive phases. Here, we investigated whether the logic of the PoA model predicted the distribution of paternity across ranks in a seasonal breeder with high reproductive synchrony over six consecutive mating seasons. We studied 18 males that resided in a group of wild Assamese macaques (Macaca assamensis) in their natural habitat at Phu Khieo Wildlife Sanctuary, Thailand, between 2006 and 2011 with 5 to 13 conceptions per season. We assessed whether mate guarding increased paternity success, described “short-term” deviations from predicted paternity distribution, and examined how these are related to the number of competitors and fertile females. We determined genetic paternity of 43 (93 %) offspring born into the study group and found reproductive skew to be relatively low with 29 % alpha male paternity in accordance with the high degree of female reproductive synchrony observed. Short-term deviations from expected paternity distribution over ranks were not explained by the number of resident males or the number of conceiving females or their interaction. Within the limits of this study, these results suggest that even if males cannot discern female fertile phases, if reproduction is seasonal, and if reproductive synchrony is high, males may also compete directly over access to females.     

Mate guarding,copulation strategies and paternity in the sex-role reversed,socially polyandrous red-necked phalarope<Emphasis Type="Italic"> Phalaropus lobatus</Emphasis>

In a recent review, Westneat and Stewart (2003) compiled evidence that extra-pair paternity results from a three-player interaction in which sexual conflict is a potent force. Sequentially polyandrous species of birds appear to fit this idea well. Earlier breeding males may attempt to use sperm storage by females to obtain paternity in their mates subsequent clutches. Later-breeding males may consequently attempt to avoid sperm competition by preferring to pair with previously unmated females. Females may bias events one way or the other. We examined the applicability of these hypotheses by studying mating behavior and paternity in red-necked phalaropes (Phalaropus lobatus), a sex-role reversed, socially polyandrous shorebird. Male red-necked phalaropes guarded mates more strongly than other shorebirds. Males increased within-pair copulation attempts during their mates fertile period, and maintained or further increased attempts towards the end of laying, suggesting an attempt to fertilize the females next clutch; these attempts were usually thwarted by the female. Paired males sought extra-pair copulations with females about to re-enter the breeding pool. Multilocus DNA fingerprinting showed that 6% of clutches (4/63) each contained one chick sired by a male other than the incubator, producing a population rate of these events of 1.7% (n=226 chicks). Male mates had full paternity in all first clutches (n=25) and 15 of 16 monogamous replacement clutches. In contrast, 3 of 6 clutches of second males contained extra-pair young likely fathered by the females previous mate. Previously mated female phalaropes may employ counter-strategies that prevent later mating males from discriminating against them. The stability of this polyandrous system, in which males provide all parental care, ultimately may depend on females providing males with eggs containing primarily genes of the incubating male, and not a previous mate.Communicated by M. Webster     

Inbreeding level does not induce female discrimination between sibs and unrelated males in guppies

Significant empirical evidence has demonstrated the importance of discriminative mate choice as a mechanism to avoid inbreeding. Incestuous mating can be avoided by recognition of kin. The guppy, Poecilia reticulata, is a livebearer with a polygamous mating system and active female choice. Despite potential inbreeding costs in the guppy, Viken et al. (Ethology 112:716–723, 2006) and Pitcher et al. (Genetica 134:137–146, 2008) have found that females do not discriminate between sibs and unrelated males. However, populations experiencing different inbreeding histories can have different levels of inbreeding avoidance, and it is possible that the lack of inbreeding avoidance observed in guppies is a consequence of using outbred fish only. Here we tested the preference of female guppies with different inbreeding coefficients, for olfactory cues of males that were either unrelated but had the same inbreeding coefficient, or were related (i.e. brother) with the same inbreeding coefficient. We found no evidence that female guppies preferred unrelated males with the same inbreeding coefficient. Moreover, inbreeding level did not influence female preference for unrelated males, suggesting that inbreeding history in a population has no influence on female discrimination of unrelated males in guppies.