Unravelling Evolutionary Dynamics of Female Sexual Cannibalism and Male Reproductive Strategies in Spiders.

Male–male competition and female mate choice act contemporaneously in the cockroach Nauphoeta cinerea and the social pheromone of males influences the outcome of both forms of sexual selection. We therefore examined the joint and separate effects of male–male competition and female mate choice to determine if the selective optima for the pheromone were the same or different. Dominant males in a newly established hierarchy mated more frequently, but not exclusively. Manipulations of the multi-component social pheromone produced by males of N. cinerea showed that both long- and close-range attraction of females by males were influenced by the quantity and composition of the pheromone. The most attractive composition, however, differed from that which was most likely to confer high status to males. Since the outcome of male–male competition can conflict with mating preferences exhibited by females, there is balancing sexual selection on the social pheromone of N. cinerea. Such balancing selection might act to maintain genetic variation in sexually selected traits. We suggest that the different forms of sexual selection conflict in N. cinerea because females prefer a blend different to that which is most effective in male–male competition in order to avoid mating with overly aggressive males.

Sperm competition is a potent driving force in evolution leading to a remarkable variety of male adaptations that prevent or reduce fertilization by rivals. An extraordinary defensive strategy against sperm competition has evolved in a number of web spiders where males break off parts of their paired genitalia in order to obstruct the copulatory openings of females (mating plug). A recent comparative analysis on the family level reports that genital damage is most frequent in species with sexual cannibalism although, as yet, a functional association between sexual cannibalism and genital damage has not been found. Using the moderately sexually cannibalistic orb-web spider Argiope lobata, we show for the first time that males cannibalized during their first copulation damaged their pedipalps with significantly higher probability (74%) than males that escaped (15%). Of all males that damaged their genitalia, 44% were able to place a genital fragment inside the copulatory opening of the female, resulting in a relatively low total plugging rate of 14%. Successful obstruction of the female copulatory opening reduced the share of paternity of subsequent males (P 2 = 0.06%), thus, indicating that genital damage may have evolved as a response to sperm competition in this species as well. However, the low incidence of successful plugging and the strong relationship between sexual cannibalism and genital damage suggest that apart from paternity protection, the nature of genital damage in A. lobata is further shaped by sexual conflict or cryptic female choice.

In most sexually reproducing organisms females obtain sperm from multiple males. Such widespread female promiscuity prolongs the operation of sexual selection after copulation, through the competition of the ejaculates of different males over fertilisation (sperm competition) and mechanisms by which females systematically bias the outcome of sperm competition (cryptic female choice – CFC). Post‐copulatory sexual selection can either consistently favour certain male or ejaculate phenotypes or certain combinations of male and female genotypes. Sperm competition and CFC drive the evolution of a diverse range of post‐copulatory strategies resulting in differential ejaculate allocation by males and differential sperm utilisation by females. The post‐copulatory reproductive strategies of each sex have considerable impact on the fitness of the opposite sex, giving rise to an intimate process of intersexual coevolution. The concept of post‐copulatory sexual selection is therefore a powerful heuristic tool to explain variation in individual fitness and the staggering variation in sexual strategies both across and within species. Key Concepts: Sexual selection, or intrasexual competition for mates and fertilisation, can continue after copulation when females mate with multiple males (polyandry). The post‐copulatory processes of sperm competition and cryptic female choice are equivalent to pre‐copulatory mate competition and female choice. Molecular and behavioural studies have demonstrated the female multiple mating is nearly ubiquitous and therefore post‐copulatory sexual selection is a major evolutionary force. Sperm competition occurs when the ejaculates of different males compete to fertilise the same set of eggs, and selects for male adaptations both to prevent and win such competition A male's relative share of paternity is increased through adaptations of sperm quantity and quality, in addition to behavioural, morphological and physiological adaptations in somatic traits. Cryptic female choice (CFC) refers to female‐driven biases in the outcome of sperm competition, which are repeatable within females. CFC and sperm competition are often difficult to distinguish because they can interact to bias sperm use. Females have a wide variety of adaptations that mediate CFC; examples include differential sperm ejection, spermicide, and differential maternal allocation. Patterns of CFC can either differ between different combinations of male and female genotypes, or be consistent among females sharing similar preferences. Post‐copulatory sexual selection can foster the maintenance of polymorphism and alternative reproductive strategies within a species. The post‐copulatory reproductive strategies of one sex can reduce the fitness of the other sex, reflecting sexual conflict over mating and fertilisation. Such conflict can fuel sexually antagonistic coevolution of post‐copulatory traits.

Mating strategies are to a large degree shaped by conflicts between the sexes, causing a rapid antagonistic coevolution of traits involved in reproduction. The view that sexual cannibalism represents a form of sexual conflict leads to the prediction of male traits that facilitate escape from cannibalistic females. A variety of traits have been suggested to serve this function in spiders, where sexual cannibalism is comparatively common. Empirical evidence, however, is virtually absent. Here we show experimentally that opportunistic mating with feeding females, which has been reported from several species of orb-weaving spiders, greatly reduces the risk of cannibalism and injury for males in the spider Nephila fenestrata. This has direct consequences for a male's fertilization success because surviving males can reduce the female's remating probability by guarding her against rivals. Although copulation with previously mated females sometimes appears to be mechanically impossible, second males that do copulate can expect to fertilize on average 64% of a female's eggs. Our results support the view that opportunistic mating may have evolved as a male tactic in a context of sexual conflict over sexual cannibalism.

Sperm competition

On parsimonious paternity and scientific rigor: a reply to Madsen

A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females

Reproduction is composed by a series of strategies performed by each sex in order to gain control over the outcome of the entire process. Males’ attempts to fertilize the females may deal with a hidden factor: the cryptic female choice , which is the females’ ability to control fertilization based on males’ sexual performance. A particular kind of reproductive strategy adopted by males of several invertebrate orders involves the transfer of substances or materials during the courtship and/or copulation, also known as nuptial gifts (NG). At least nine spider families have representatives that rely on the transfer of NG, all of them classified as oral gifts. Given its appeal in broad areas of behavioral ecology, NG received great attention in terms of their role in determining the outcome of sexual interactions, but little effort was applied toward the integrate analysis of the entire courtship/copulatory process. NGs are obviously just a stage of the entire mate choice process, and the empirical data available supports the idea of sexual conflict. However, I defend that only an integrated analysis will allow us to understand if NG does play some role as a source of information for cryptic female choice, or if it still remains as a way that males found to mitigate the sexual conflict issues.

We reviewed the recent information on various aspects of courtship in insects. Chemical cues initiate courtship due to specialized olfactory and gustatory receptors present on antennae and entire body parts of insects. Males usually court females using various visual cues, acoustic signals, tactile stimuli, nuptial gifts, etc. Certain male insects compose and sing calling songs (for mate location) and courtship songs (after mate location and recognition), which sometimes end up in duets when their female partners respond. Through tactile stimulation males examine, embrace, tap, fan, bump, drum, and brush females. Males give exogenous and endogenous nuptial gifts to their partners, viz. food items, salivary gland secretions, carrions, plant products, spermatophores, free ejaculates, and even portion of their body parts. Abnormal courtship in form of same sex courtship, sexual cannibalism, and heterospecific courtship are also prevalent. Proximate causes of courtship include chemical signals, operational sex ratio, female mating preferences, body size, and overcrowding during immature development of insects. Ultimate evolutionary causes of courtship are male sexual traits, intra sexual competition, cryptic female choice, and sexual conflict. Insects court their partners with both honest and dishonest signals regarding information about their internal and external biological traits. Such signals have both benefits and costs. Temperature and light are important environmental factors that affect courtship behaviour. Sexual selection drives evolution of diversified courtship displays, particularly, calling and courtship songs, duets, and secondary sexual traits.

Evolutionary Significance of Sexual Cannibalism

The renaissance of interest in sexual selection during the last decades has fuelled an extraordinary increase of scientific papers on the subject in spiders. Research has focused both on the process of sexual selection itself, for example on the signals and various modalities involved, and on the patterns, that is the outcome of mate choice and competition depending on certain parameters. Sexual selection has most clearly been demonstrated in cases involving visual and acoustical signals but most spiders are myopic and mute, relying rather on vibrations, chemical and tactile stimuli. This review argues that research has been biased towards modalities that are relatively easily accessible to the human observer. Circumstantial and comparative evidence indicates that sexual selection working via substrate-borne vibrations and tactile as well as chemical stimuli may be common and widespread in spiders. Pattern-oriented research has focused on several phenomena for which spiders offer excellent model objects, like sexual size dimorphism, nuptial feeding, sexual cannibalism, and sperm competition. The accumulating evidence argues for a highly complex set of explanations for seemingly uniform patterns like size dimorphism and sexual cannibalism. Sexual selection appears involved as well as natural selection and mechanisms that are adaptive in other contexts only. Sperm competition has resulted in a plethora of morphological and behavioural adaptations, and simplistic models like those linking reproductive morphology with behaviour and sperm priority patterns in a straightforward way are being replaced by complex models involving an array of parameters. Male mating costs are increasingly being documented in spiders, and sexual selection by male mate choice is discussed as a potential result. Research on sexual selection in spiders has come a long way since Darwin, whose spider examples are reanalysed in the context of contemporary knowledge, but the same biases and methodological constraints have persisted almost unchanged through the current boom of research.

How male insects score

Several hypotheses have been proposed for the evolution of sexual cannibalism by females. Newman and Elgar (1991) suggested that sexual cannibalism prior to mating by virgin female spiders may have evolved as a result of female foraging considerations. According to this model, an adult female's decision to mate or cannibalize a courting male should be based on an assessment of the male's value as a meal versus his value as a mate. The current study provides an empirical test of the assumptions and predictions of this model in the sexually cannibalistic fishing spider. Adult females were subjected to different food treatments, and exposed to adult males in the laboratory. However, only one of the assumptions of the model and none of its five predictions were upheld. We failed to find any effects of female foraging, female mating status, female size, male size or time of the season on females' behaviour towards courting males. Females behaved stereotypically, and many females were left unmated despite numerous mating opportunities. We also demonstrate costs of sexual cannibalism in a natural population. We propose that the act of sexual cannibalism in the fishing spider is non-adaptive, and develop a model for the evolution of premating sexual cannibalism in spiders based on genetic constraints. According to this hypothesis, sexual cannibalism by adult females may have evolved as an indirect result of selection for high and non-discriminate aggression during previous ontogenetic stages. Genetic covariance between different components of aggressive behaviour may constrain the degree to which (1) juvenile and adult aggression and/or (2) aggression towards conspecifics and heterospecifics can vary independently. We briefly review the support for our model, and suggest several critical tests that may be used to assess the assumptions and predictions of the model.

Spiders have long been noted as classic examples of sexual behavior among arachnids, including extreme sexual dimorphism in some groups, and behavioral adaptations to diverse mating patterns. In recent decades, studies on the biology of Neotropical spiders have offered novel information on processes related to reproductive biology, including sexual selection. The present chapter synthesizes the large amount of knowledge on sexual selection and associated subjects in spiders from the Neotropics. Some of the groups considered in this review are mygalomorphs, lycosids and related, orb-weaving species, tetragnathids, social species, pholcids, and oonopids, among others. Concepts, patterns, mechanisms, and prospects on different areas of sexual selection are shown in detail for all these groups. In particular, here we highlight selected examples of the different contexts in which male–female interactions occur, such as mate choice, sexual cannibalism, sperm competition, and cryptic female choice. We outline the potential evolutionary consequences according to those contexts, with a final selection of model groups for specific experimental and comparative investigations.

The field of sexual selection has been historically dominated by a stereotyped view of the sexual roles, with competing males and selective females, but in recent decades there has been a paradigm switch, with the emergence and dominance of the concept of sexual conflict. Put simply, there is sexual conflict when the optimum value for a trait (or a group of traits) is different for females and males. Although the recent literature mainly considers sexual conflict as a process separate from the other well-known processes in the field of postcopulatory sexual selection (sperm competition and cryptic female choice), our approach is that sexual conflict is the consequence of several pressures related to natural and sexual selection, and not a process by itself. Therefore, here we consider sexual conflict as a part of a continuum of sexual selection mechanisms. We concentrate on the effects of sexual conflict on reproductive behaviour of three groups of aquatic insects, whose habitats differ markedly, water striders, odonates and diving beetles, but also include some examples of studies addressing sexual conflict in other groups of aquatic insects. Our hypothesis is that the dimensional structure of the habitat will affect the intensity of sexual conflict over mating rate, copulation duration and postcopulatory guarding. There is abundant evidence and comprehensive reviews of the conflict over mating rates in water striders, odonates and, to a lesser degree, diving beetles. The bi-dimensionality of the water surface allows an easy monopolisation of females by males in this microhabitat, and water striders conform to this rule, so that the commonest mating system is characterised by strong conflicts and struggles before and after copulation. For animals like odonates, which are fast fliers and can use diverse terrestrial microhabitats, the opportunities for males to force females to copulate are certainly limited. In the case of diving beetles, the situation seems more favourable for the females, as they could control male approaches by hiding easily in the vegetation, or even in the case of extreme male density they could fly away and move to a different water body. The sexual conflict over mating duration is also intense in water striders, and also relevant in the other reviewed groups. In the field of postcopulatory conflicts, odonates have offered the best examples of male adaptations and female counter-adaptations, which are even more elaborated when studying the evolution of genitalia. We end by summarising our main conclusions and propose some ideas for future work. We stress that a comprehensive understanding of sexual conflicts in animals requires the study of both male and female anatomies, as well as their behaviours, avoiding assumptions or gender stereotypes, which have historically biased research to a male-view approach.