Forced Copulation Research Articles

Female choice, male dominance and condition-related traits in the polygynous subterranean rodent Ctenomys talarum

Ctenomys talarum is a solitary and highly territorial species in which dominant males aggressively deter other males and monopolize reproductive activity. Female preference for dominant males is not easy to assess due to coercive mating by males. Hence, we aimed to answer if behavioural dominance and several condition-related traits like testosterone and cortisol levels, endoparasite load, and hematocrit volume may affect female preference when they have the opportunity to exert it. We designed a laboratory experiment using wild-caught C. talarum and employed a combined approach involving behavioural observations and the measurements of parameters of physical condition. We staged dyadic encounters between males to determine dominance index and then analyzed female preference towards tethered males (n=15) or their odours (n=18). Male dominance did not affect female preferences when odours were presented. When two tethered males were offered, females preferred those with higher dominance index. Preference of females for dominant males would mainly represent indirect benefits. Females did not show preference for males in relation to any physiological trait evaluated. Dominance was found negatively related to cortisol levels, probably avoiding the glucocorticoids-related costs, and positively related to parasite diversity, since they could tolerate it without impairing their health.

Patterns of intraspecific aggression inferred from injuries in an aquatic turtle with male-biased size dimorphism

Patterns of sexual size dimorphism (SSD) in turtles are correlated with ecological mode, and it has been hypothesized that mating systems are also shaped by ecological mode. Male combat and coercive mating are competing explanations for male-biased SSD, but are difficult to assess empirically in aquatic species with cryptic behaviour. We quantified SSD and compiled observations of putative combat wounds collected from over 500 captures of Snapping Turtles (Chelydra serpentina (L., 1758)) in Algonquin Provincial Park, Ontario, to test hypotheses of mate competition and coercion. We found that both sex and body size were important predictors of risk of wounding, consistent with the hypothesis that male–male sexual competition is the primary driver of intraspecific aggression. Low wounding rates among females suggests that resource competition and coercive mating are not important causes of injuries. The risk of wounding increased monotonically with body size in adult males but not in adult females, and small males were less likely to be injured, suggesting that they employ a risk-averse strategy by avoiding direct competition for mates. There was no evidence of asymptotic or decreasing wounding probability in the largest males, which is consistent with the hypothesis that large males compete most intensively to monopolize mates.

Dramatic Fighting by Male Cuttlefish for a Female Mate.

Male cuttlefish compete for females with a repertoire of visually dramatic behaviors. Laboratory experiments have explored this system in Sepia officinalis, but corroborative field data have eluded collection attempts by many researchers. While scuba diving in Turkey, we fortuitously filmed an intense sequence of consort/intruder behaviors in which the consort lost and then regained his female mate from the intruder. These agonistic bouts escalated in stages, leading to fast dramatic expression of the elaborate intense zebra display and culminating in biting and inking as the intruder male attempted a forced copulation of the female. When analyzed in the context of game theory, the patterns of fighting behavior were more consistent with mutual assessment than self-assessment of fighting ability. Additional observations of these behaviors in nature are needed to conclusively determine which models best represent conflict resolution, but our field observations agree with laboratory findings and provide a valuable perspective.

The association between male-biased sex ratio and indicators of stress in red-spotted newts

In populations with a male-biased operational sex ratio, coercive mating by males can have fitness consequences for females. One component of reduced fitness for females in populations with a male-biased OSR may be greater activation of the stress response, resulting in higher corticosterone release rates (CORT; a glucocorticoid stress hormone in amphibians). We test the hypothesis that a male-biased sex ratio affects female activity and release rates of CORT and testosterone (T) in male and female red-spotted newts (Notophthalmus viridescens). First, we evaluated if chemical cues from a male-biased sex ratio affect activity and CORT release rates in females. We predicted that females exposed to chemical cues of three males would be less active and have higher CORT release rates than those exposed to chemical cues of one male. Second, we measured CORT release rates of red-spotted newts in field enclosures with either a male-biased or a female-biased sex ratio. We predicted that females in the male-biased treatment would have higher CORT and T release rates than those in a female-biased treatment, owing to higher levels of male harassment. We also predicted that males would have higher CORT and T release rates in male-biased treatments due to higher levels of male-male competition. Females were not less active in response to chemical cues from more males over fewer males, but there was a positive relationship between female activity and CORT when they were exposed to the cues of three males. We also found that females, but not males, in the male-biased sex ratio treatment had higher CORT and T release rates than those in the female-biased treatment. Our results support the hypothesis that a male-biased sex ratio leads to a higher stress response, which may underlie the observed decrease in immune function and body condition in previous work exposing female red-spotted newts to a male-biased sex ratio. This study furthers our understanding of the mechanistic basis for costs associated with a male-biased sex ratio in a pond-breeding amphibian.

Antennation and sexual performance of male digger wasps Sphex ingens Smith (Hymenoptera: Sphecidae)

ABSTRACTAntennation can play several roles in hymenopteran copulation, mainly in wasps. The digger wasp Sphex ingens Smith has a very peculiar sexual behaviour, in which forced copulation is a striking element. However, communication through antennation during the pre-copulation and copulation phases and the relationship between the sexual performance of males and the final result of copulation require further clarification. The sexual behaviour of wild populations of S. ingens was filmed during the breeding season in a site between the beaches Meros and Aventureiro, Ilha Grande, southeastern Brazil. We assessed antennation behaviour, courtship duration, sexual performance, and genital clasping. Only successful males had the genital clasping assessed. Evidence found so far points out that the successful males showed better sexual performance – that is, they antennated more in a shorter courtship duration. Also, genital clasping in successful males did not depend on antennation, courtship duration, or sexual performance. Our results shed light on some aspects of the sexual behaviour of wasps, as they explain part of the sexual selection mechanisms adopted by the species.

Multiple paternity in a viviparous toad with internal fertilisation.

Anurans are renowned for a high diversity of reproductive modes, but less than 1 % of species exhibit internal fertilisation followed by viviparity. In the live-bearing West African Nimba toad (Nimbaphrynoides occidentalis), females produce yolk-poor eggs and internally nourish their young after fertilisation. Birth of fully developed juveniles takes place after 9 months. In the present study, we used genetic markers (eight microsatellite loci) to assign the paternity of litters of 12 females comprising on average 9.7 juveniles. In 9 out of 12 families (75 %), a single sire was sufficient; in three families (25 %), more than one sire was necessary to explain the observed genotypes in each family. These findings are backed up with field observations of male resource defence (underground cavities in which mating takes place) as well as coercive mating attempts, suggesting that the observed moderate level of multiple paternity in a species without distinct sperm storage organs is governed by a balance of female mate choice and male reproductive strategies.

Male Reproductive Morphology Across Latitudinal Clines and Under Long-Term Female Sex-Ratio Bias.

SynopsisRecent work in evolutionary ecology has capitalized on the species-specific, rapidly evolving nature of male reproductive traits, but it is unclear how the strength of sexual selection mechanisms, such as female choice and intersexual conflict, changes with ecological factors-shifts in latitude, elevation, and sex-ratio. Marginal habitats, such as those found at high elevation or latitude, might be expected to exert energetic hardships on males such that they do not invest heavily in reproductive structures. Conversely, males in these habitats may adapt to limited breeding opportunities, evolving morphologies with efficacy in antagonistic mating. Sex-ratio biases elicited by facultative parthenogenesis may also signal increasing selective pressure for reproductive organs that improve coercion ability, as males must capitalize on mating opportunities when females have alternate reproductive options. We studied the reproductive organs of males of five species of a group of polygynandrous Japanese harvestmen, collected from populations that varied in their elevation, latitude, and observed male: female ratio. Morphological data were analyzed with modern comparative methods, using a phylogenomic framework built with molecular data from double-digest restriction associated DNA sequencing. Although no features with hypothesized utility in coercive mating significantly covaried with elevational change, penis length was found to decrease with increasing latitude, supporting the existence of physiological constraints in marginal habitats. We also found males of parthenogenetic species, with primarily female-biased populations, had potentially greater precopulatory clasping ability, as compared to males of non-parthenogenetic species with more even sex-ratios. Ultimately, our findings suggest long-term sex-ratio biases are one of many factors with the potential to influence evolution of primary and secondary reproductive morphology.

Do Female Western Mosquitofish,Gambusia affinis,Prefer Ornaments That Males Lack?

AbstractSome species in the family Poeciliidae are known for extravagant male ornaments and courtship behavior (e.g., guppies), but the majority of poeciliids are characterized by coercive male copulation attempts that seem to circumvent female choice. In some lineages with male ornaments, female sensory bias may have preceded the evolution of corresponding male signals. We examined female preferences for colorful ornaments in Western mosquitofish,Gambusia affinis, in which males lack ornamentation and reproduce primarily through coercive mating attempts. We found that females exhibited a positional affinity for males that were artificially ornamented with blue coloration over males that had been treated with a transparent ornament. Females exhibited the opposite effect for males treated with red ornaments. In contrast, focal females did not exhibit behavioral discrimination between two live stimulus females or two models (silver fishing lures) with blue vs. transparent ornaments. This suggests a sexual context for female discrimination between males based on ornament color and whether an ornament was present. Because tribe Gambusiini is the basal branch of family Poeciliidae, the results of this study are consistent with the hypothesis that female responsiveness to male coloration is the ancestral poeciliid character state.

Male coercive mating in externally fertilizing species: male coercion, female reluctance and explanation for female acceptance.

Male coercive mating exerts a strong evolutionary pressure on mating-related traits of both sexes. However, it is extremely rare in externally fertilizing species probably because the male mating behaviour is incomplete until females release their eggs. Here we showed that males of the externally fertilizing fish Rhabdoblennius nitidus coercively confine females to the nests until spawning, and investigated why females accept male coercive mating. The females entered the males’ nests following male courtship displays, but they usually tried to escape when there were no eggs because males tended to cannibalize all the eggs when there were few. Most males that used small, tight nests acquired new eggs but with experimentally enlarged nests, 90% of the males without eggs failed to confine the females. Spawning tended to occur during the early/late spawning period in nests with no eggs (i.e. male coercive mating). In the nests where the first eggs were deposited in the early period, subsequent matings with other females were more likely to occur, whereas in the late period, most parental care of the eggs failed without additional matings. The females that spawned in the late period may have been compelled to accept male coercive mating due to time constraints.

The ecological costs to females in a system with allied sexual coercion

Sexual coercion results from extreme conflict over mating. As a male strategy to overcome female resistance, coercion can impose fitness costs on females. Among mammals, most cases involve single males or temporary coalitions, with allied aggression towards females being rare. Among Shark Bay bottlenose dolphins, Tursiops cf. aduncus, male alliances harass, guard and consort with females to obtain mating access, which has known physical costs to females. However, the behavioural and ecological costs of sexual coercion to females remain largely unexplored. Given the importance of individual differences in ranging and habitat use for dolphin foraging ecology, social networks and fitness, we hypothesized that male coercion also imposes ecological costs on females. Using 25 years of longitudinal data, we examined how adult male presence relates to female space use, and we found that females (N = 32) altered their ranging when associating with adult males but also when they were cycling. Additionally, females reduced the use of their primary (preferred) habitat when with males, but cycling had no effect. Ranging shifts were slightly greater for males than for females when they were together, but only for females did this alter their spatial ecology. While it is also possible that males follow fertile females and/or that females move to avoid males, the well-documented coercive mating system suggests that males, as part of their coercive mating tactics, sequester females to areas that females would not otherwise occupy. Our results show that in a coercive mating system, males can alter females' basic behavioural ecology, and suggest that males spatially sequester individual females via allied consortships.

On the evolutionary stability of male harassment in a coercive mating game

In many animals, males employ coercive mating strategies to help them maximize their expected number of offspring. In such systems, selection will favor behavioral adaptations in females that help them mitigate harassment costs and maximize their reproductive fitness. Previously, Bokides et al. [1] presented a model showing how male harassment strategies can co-evolve with female habitat preferences in a mating game. Their results indicated that if females dispersed freely between habitats where males were present and where males were excluded, selection could favor males who strategically harassed at high (or low) levels, depending on the proximity of their phenotype to a threshold level $h^*$. This article is a continuation of that work addressing the questions of stability at equilibria where males harass at the threshold level (i.e., $h^*$). We show these states are both locally and globally asymptotically stable. Further, we argue based on these results that $h^*$ is an evolutionary stable male harassment level at which females will be ideally distributed to match the resource quality and social environments of their alternative habitats.

The potential for disruptive selection on growth rates across genetically influenced alternative reproductive tactics

A trade-off between survival to sexual maturity and mating success is common across alternative reproductive tactics (ARTs), and can lead to tactical disruptive selection on shared traits (i.e. positive selection gradient in one tactic, and negative selection gradient in another). We were interested in examining the theoretical possibility of tactical disruptive selection on intrinsic growth rate. The male ARTs in Xiphophorus multilineatus express two distinct life histories: “courters” optimize mating success by maturing later at larger size and coaxing females to mate, while “sneakers” optimize survival to sexual maturity by maturing earlier at a smaller size, using both coaxing and coercive mating behaviors. In addition to differences in mating behaviors, body length, body depth, and the pigment pattern vertical bars, courter males grow faster than sneaker males. We present a new hypothesis for differences in growth rates between genetically influenced ARTs. The “growth-maturity optimization” hypothesis suggests that ARTs with differences in the probability of surviving to sexual maturity may have different optimal growth rates, leading to tactical disruptive selection. We also present a simple model to suggest that when considering both a cost and benefit to faster growth, tactical disruptive selection on growth rates is theoretically possible. In our model, the value that determines when tactical disruptive selection on growth rate will occur is the increase in probability of survival to sexual maturity gained through faster growth multiplied by the cost of faster growth (reduced longevity). Finally, we present empirical evidence to support the prediction that faster growth has a cost in X. multilineatus: in a controlled laboratory setting, courter males that did not survive 1.2 years past sexual maturity grew faster as juveniles (14–70 days) than those that survived.

Social interactions generate mutually reinforcing selection for male aggression in Lake Eyre dragons

Fighting ability is generally assumed to predict male reproductive success; yet the mechanisms responsible for this relationship are seldom known. Competitively superior males may monopolize access to females, be preferred by females, invest more into courtship, or employ more coercive mating tactics. Differentiating these alternatives is essential to understand the interaction between male–male competition and female mate choice, and their influence on the evolution of male traits such as aggression. We tested whether male fighting ability, body size, courtship, or coercive behavior in intersexual interactions predict copulation success in the Australian Lake Eyre dragon lizard, Ctenophorus maculosus. Males with superior fighting ability had higher mating success; however, male harassment (biting and chasing) was a much stronger predictor of copulation, likely because aggressive males are able to overcome female resistance. Better fighters also copulated for longer, which may increase sperm transfer and/or fertilization success. Conversely, courtship effort (head-bobs) decreased copulation success, but only for small males. Females were no less likely to reject males with higher fighting ability, suggesting that females do not prefer these males. Furthermore, males with superior fighting ability were no more or less likely to court or harass females. Instead, both fighting ability and aggression towards females independently increased mating success, potentially generating mutually reinforcing selection on male aggression.

The effect of sperm production and mate availability on patterns of alternative mating tactics in the guppy

Theory predicts that in polyandrous species males that invest more in traits enhancing postcopulatory success should have less energy to invest in mating acquisition, leading to trade-offs between pre- and post-copulatory episodes of sexual selection. Although such trade-offs are well studied, the potential constraints that postcopulatory sexual selection imposes on alternative mating tactics are rarely considered. In guppies, Poecilia reticulata , individual males can obtain matings by performing energetically costly courtship displays or by using less costly forced copulations. In this study we manipulated a component of social environment (namely, the presence of females) to experimentally elevate sperm production in males. We found that male guppies rapidly compensated by reducing their reliance on courtship in favour of forced matings. As both tactics differ in mating and fertilization success, the consequences of this trade-off may have important ramifications for male reproductive fitness.

Predictors of male insemination success in the mosquitofish (Gambusia holbrooki).

Identifying targets of selection is key to understanding the evolution of sexually selected behavioral and morphological traits. Many animals have coercive mating, yet little is known about whether and how mate choice operates when these are the dominant mating tactic. Here, we use multivariate selection analysis to examine the direction and shape of selection on male insemination success in the mosquitofish (Gambusia holbrooki). We found direct selection on only one of five measured traits, but correlational selection involving all five traits. Larger males with longer gonopodia and with intermediate sperm counts were more likely to inseminate females than smaller males with shorter gonopodia and extreme sperm counts. Our results highlight the need to investigate sexual selection using a multivariate framework even in species that lack complex sexual signals. Further, female choice appears to be important in driving the evolution of male sexual traits in this species where sexual coercion is the dominant mating tactic.

What the direction of matings can tell us of hybridisation mechanisms in ducks

Interspecific hybridisation is common amongst birds and is associated with diverse costs and benefits. Several mechanisms are thought to promote hybridisation, including heterospecific mate choice, species recognition errors and interspecific forced copulations. Discriminating between these mechanisms is often problematic due to difficulties in observing interspecies copulations in the wild. The directionality of hybridisation may, however, provide some insights into which mechanisms are operating. For example, matings may be unidirectional when females prefer to mate with heterospecific males with a specific trait, such as higher dominance or a supernormal stimulus. In contrast, bidirectional hybridisation is more likely when other mechanisms, such as heterospecific imprinting as a result of brood mixing, are operating. We here characterise the direction of matings between Grey Teal (Anas gracilis) x Pacific Black Duck (A. superciliosa) hybrids. By sequencing a fragment of the maternally inherited mitochondrial DNA, we show that hybridisation occurs bidirectionally between these species. This suggests that a female preference does not exist in both species for a specific male trait of only one species. We suggest that errors in species recognition are improbable and that heterospecific mate choice, possibly due to brood mixing, may more likely promote hybridisation between Grey Teals and Pacific Black Ducks.

Establishment of a free-mating, long-standing and highly productive laboratory colony of Anopheles darlingi from the Peruvian Amazon.

BackgroundAnopheles darlingi is the main malaria vector in the Amazon region and is among the most efficient malaria vectors worldwide. However, due to the lack of a well-established laboratory colony, key control-relevant aspects of the bionomics, behaviour, genetics, and vector-parasite relationships of An. darlingi remain unknown. Here, biological parameters that had been successful in initiating other Anopheles colonies were optimized and improved for An. darlingi, with the aim of establish a free-mating, stable, and highly productive laboratory colony.MethodsWild An. darlingi adult females were field collected from Zungarococha, Loreto Department, Peru (03°49′32.40″S, 73°21′00.08″W), and taken to the NAMRU-6 Insectary in Iquitos where F1 offspring were produced and reared. Natural copulation was successfully induced in F1 adults under a thermoperiod of 30 ± 1 °C during the day and 25 ± 1 °C at night, and with a 30-min LED light stimulation period at dusk. Oviposition success was enhanced using egg-laying containers with a dark-coloured surface. Larval feeding regimes were standardized for optimal larval development. Optimized copulation induction methods were used to facilitate mating in An. darlingi until the F10 generation. No copulation induction assistance was needed in subsequent generations.ResultsIn 19 generations, the An. darlingi colony produced a total of 763,775 eggs; 441,124 larvae; 248,041 pupae; and 231,591 adults. A mean of 0.56 sexual encounters/female/cage (n = 36 cages) was recorded across the first ten generations (F1-F10). A mean insemination rate of 54.7 % (n = 5,907 females) ranging from 43.6 % (F2) to 66.6 % (F10) was recorded across nine generations (F2-F10). Free-mating was casually observed in the F8 generation, and subsequently confirmed in the F9 and F10 generations; comparable insemination rates and egg laying between stimulated (51.6 %, 12.9 eggs/female), and non-stimulated (52.3 %, 11.2 eggs/female) females were recorded. The time from egg to adult development ranged from 10 to 20 days. Moreover, the colony was relocated to a new laboratory within Iquitos in the F14 generation without any noted changes in its productivity. By March 2015, the An. darlingi colony has been successfully reared to the F26 generation.ConclusionsThis constitutes the first report of a free-mating, highly productive, and long-standing An. darlingi laboratory colony established through natural copulation induction, which will support critical malaria research. This rearing methodology may be a transferable, cost-effective alternative to labour-intensive forced mating practices widely used in maintaining other Anopheles colonies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-015-0733-0) contains supplementary material, which is available to authorized users.

Females Choose Mates Based on Genetic Relatedness in a Small Dasyurid Marsupial, the Agile Antechinus (Antechinus agilis).

Females in a variety of taxa mate with more than one male during a single oestrus and exhibit mate preferences for genetically compatible males, but the influence of female mate choice on siring success is not clearly understood. Whether females choose to mate with more than one male or endure forced copulations is also often unknown. Here, we examined the effects of genetic relatedness on female mate choice and siring success in a small semelparous carnivorous marsupial, the agile antechinus (Antechinus agilis), during two consecutive breeding seasons. Experimental trials were conducted in captivity over periods of 72 hours using interconnected enclosures in which female antechinus could choose to access any of four separated males, but males were only able to access females that entered their quarters. Females had access to two genetically similar and two genetically dissimilar males simultaneously and all behavioural interactions were observed and scored from continuous video recordings. Genetic similarity between mates and paternity of young was determined by microsatellite analyses. Some females chose to enter and mate with more than one male during a single oestrus period. Although females investigated all males, they spent significantly more time visiting, and mated more times with, genetically dissimilar males. Males that were genetically dissimilar to the female sired 88% of subsequent offspring. Whilst males mated readily with most females, they rejected the advances of some receptive females, indicating a previously unexpected level of male mate choice. The results show that genetic relatedness between mates has a significant influence on mate choice, breeding and siring success in the agile antechinus.

Reproductive behaviour of three species of freshwater crabs of the family Trichodactylidae (Crustacea: Decapoda) including forced copulation by males

This report includes a detailed description of the reproductive behaviour of the freshwater crab Zilchiopsis collastinensis in the family Trichodactylidae and some observations on two other genera. It presents observations on the courtship, copulation, spawning, incubation and maternal care in Z. collastinensis. No discernible courtship behaviour occurred. We found instead that forced copulation is practised by males. Z. collastinensis copulations were observed in between April and October, for Dilocarcinus pagei between January and August, and throughout the year for Trichodactylus borellianus. The spawning behaviour of all of the species observed took place out of the water. Incubation lasted between 46 and 62 days in D. pagei, 37 and 41 days in Z. collastinensis and 8 and 12 days in T. borellianus. The number of juveniles carried by each ovigerous female ranged from 651 ± 172 in Z. collastinensis, through 582 ± 8 in D. pagei to 63 ± 33 in T. borellianus. The results support the proposition that members of the family Trichodactylidae, comprising exclusively endemic freshwater crabs, have evolved unusual adaptive reproductive behaviours to optimize their reproductive fitness in unstable environments.

Exploring simultaneous allocation to mating effort, sperm production, and body growth in male guppies

In several species, males increase their mating and sperm investment in the presence of unfamiliar females, the so-called Coolidge effect. Such an elevated reproductive effort is expected to be associated with a decreased investment in other costly traits, such as somatic growth and maintenance. How precopulatory, postcopulatory, and somatic investments interact one with each other, however, has been rarely evaluated simultaneously. We used the guppy (Poecilia reticulata), a polyandrous livebearing fish with alternative male mating tactics, to compare these 3 investments between males whose encounter rate with unfamiliar females was experimentally maintained at either high (high mate encounter rate [HER]) or low rate (low mate encounter rate [LER]) for 4 months. At the end of this period, HER males showed an increased sperm production as compared with their LER counterparts. This increment was accompanied with a reduction in the time spent following the female and by a shift from costly courtship displays to gonopodial thrusting, a less expensive coercive mating tactic. This effect may indicate a trade-off between these 2 components of male reproductive investment or may reflect a change in male optimal reproductive strategy associated with different mate encounter rate. In contrast, body growth was positively correlated with the increase in sperm production, and did not differ between experimental groups. Collectively, these results suggest that males did not vary their overall reproductive investment in response to their encounter rate with unfamiliar females, but differed significantly in the amount of resources available individually.