Mating Interactions Research Articles

Temperature impacts all behavioral interactions during insect and arachnid reproduction.

Temperature shapes the processes and outcomes of behaviors that occur throughout the progression of insect and arachnid mating interactions and reproduction. Here, we highlight how temperature impacts precopulatory activity levels, competition among rivals, communication with potential mates, and the relative costs and benefits of mating. We review how both the prevailing temperature conditions during reproductive activity and the temperatures experienced early in life influence mating-related behavior. To effectively predict the consequences of global warming for insect and arachnid mating behavior, we advocate for future work that universally integrates a function-valued approach to measuring thermal sensitivity. A function-valued approach will be especially useful for understanding how fine-scale temperature variation shapes current and future selection on mating interactions.

Reproductive interference hampers species coexistence despite conspecific sperm precedence.

Negative interspecific mating interactions, known as reproductive interference, can hamper species coexistence in a local patch and promote niche partitioning or geographical segregation of closely related species. Conspecific sperm precedence (CSP), which occurs when females that have mated with both conspecific and heterospecific males preferentially use conspecific sperm for fertilization, might contribute to species coexistence by mitigating the costs of interspecific mating and hybridization. We discussed whether two species exhibiting CSP can coexist in a local environment in the presence of reproductive interference. First, using a behaviorally explicit mathematical model, we demonstrated that two species characterized by negative mating interactions are unlikely to coexist because the costs of reproductive interference, such as loss of mating opportunity with conspecific partners, are inevitably incurred when individuals of both species are present. Second, we experimentally examined differences in mating activity and preference in two Harmonia ladybird species known to exhibit CSP. These behavioral differences may lead to local extinction of H. yedoensis because of reproductive interference by H. axyridis. This prediction is consistent with field observations that H. axyridis uses various food sources and habitats whereas H. yedoensis is confined to a less preferred prey item and a pine tree habitat. Finally, by a comparative approach, we observed that niche partitioning or parapatric distribution, but not sympatric coexistence in the same habitat, is maintained between species with CSP belonging to a wide range of taxa, including vertebrates and invertebrates living in aquatic or terrestrial environments. Taken together, it is possible that reproductive interference may destabilize local coexistence even in closely related species that exhibit CSP.

Mating and starvation modulate feeding and host-seeking responses in female bed bugs, Cimex lectularius

Reproductive fitness and survival are enhanced by adaptive behaviors that are modulated by internal physiological states and external social contexts. The common bed bug, Cimex lectularius, is an obligate hematophagous ectoparasite that requires host blood for growth, development, and reproduction. We investigated how mating, starvation and social interactions affect host-seeking, blood feeding, oviposition, and survival of female bed bugs. The percentage of females that fed and the amount of blood they ingested were greater in mated females (90–100%) than in unmated females (48–60%). Mating state also modulated the female’s orientation towards human skin odor in an olfactometer; more mated (69%) than unmated (23%) females responded to human odors. The response rate of unmated females (60%) to skin odor increased with longer starvation period, while the opposite pattern was observed in mated females (20%). Although fecundity after a single blood meal was unaffected by long or short residence and interaction with males, females subjected to frequent copulation attempts had lower survivorship and lifespan than females housed with males for only 24 h. Taken together, these results indicate that by adaptively and coordinately expressing behaviors based on the internal physiological state, females maximize their survival and reproductive fitness.

A grave drum at rocky springs: the vocalization of Bokermannohyla alvarengai (Anura: Hylidae) from the Espinhaço Range, southeastern Brazil, with notes on its natural history.

Communication in anurans is mediated mainly by acoustic signals, which are relevant for mating, territoriality, and other social interactions (Wells 2007). Although these signals are usually conspicuous and relatively stereotyped, some Neotropical frogs display noticeable diversity and complexity in their calls. For instance, Bokermannohyla, a genus of gladiator treefrog from the Atlantic Forest, Cerrado, and Caatinga Biomes of Brazil, often have complex vocal repertoires (Carvalho et al. 2012; Nali Prado 2014), whilst some congeners have simple and stereotyped calls emitted continuously (Carvalho et al. 2013; Taucce et al. 2015; Giaretta et al. 2016; Rocha et al. 2016).

Experimentally altered male mating behaviour affects offspring exploratory behaviour via nongenetic paternal effects

Evidence is emerging that fathers can have nongenetic effects on the phenotypes of their offspring. Most studies have focused on the role that nongenetic modifications to sperm can have on offspring phenotype; however, fathers can also have nongenetic effects on offspring through their interactions with females, called female-mediated paternal effects. These effects can occur in situations where male phenotype, e.g. behaviour or morphology, affects female stress and/or provisioning of offspring. These effects are potentially widespread, but few studies have explicitly investigated the role of female-mediated paternal effects on offspring phenotype. Here, we asked if male mating interactions can affect offspring via female mediated paternal effects in the Trinidadian guppy, Poecilia reticulata. To do this, we manipulated mating behaviour by: (i) administering a drug known to affect the neurotransmitter dopamine, and (ii) varying the familiarity of potential mates, which affects attractiveness in this species. With these treatments, we successfully manipulated the mating behaviour of male guppies and female preference for those males. Further, we found significant effects of sire mating behaviour, sire drug treatment, and parental familiarity status on behavioural measures of offspring anxiety in response to a novel object. Because Control offspring of ‘familiar’ and ‘unfamiliar’ pairs differed in their behaviour, our results cannot be solely attributed to potential nongenetic modifications to sperm caused by the drug. These results emphasize the importance of female-mediated paternal effects, including those caused by altered male mating behaviour, in shaping offspring phenotype.

Mutual mate choice and its benefits for both sexes

In mating interactions, it is common in nature for both sexes to choose simultaneously. However, this mutual mate choice and its consequences for progeny has received relatively little study; an approach where both male and female condition is manipulated is thus desirable. We compared both sexes’ preferences in Tenebrio molitor beetles when individual condition varied (healthy vs infected with a fungus), and observed the direct benefits of those preferences. We predicted that: (a) females and males in good condition would prefer high quality mates; (b) preferences would be weaker when the choosing individual is in poor condition (and thus less selective given, for example, time and energetic constrains); and, (c) high quality mates would lay a larger number of total eggs and/or viable eggs than low quality mates. We found that both males and females in good condition were not more likely to choose mates that were also in good condition. However, poor-condition animals were more likely to prefer similar quality animals, while high-condition animals did not necessarily prefer mates of similar condition. Choosing sick males or females had a negative impact on egg number and viability. Our results suggest a non-adaptive mate choice in this species. Possibly, a deteriorated condition may drive individuals to invest more in attracting mates, because their chances of surviving the infection are very low. However, we do not discount the possibility that the fungus is manipulating individuals to increase its transmission during mating.

Sex and death.

Sexual interactions negatively impact health and longevity in many species across the animal kingdom. C. elegans has been established as a good model to study how mating and intense sexual interactions influence longevity of the individuals. In this chapter, we review the most recent discoveries in this field. We first describe the phenotypes caused by intense mating, including shrinking, fat loss, and glycogen loss. We then describe three major mechanisms underlying mating-induced killing: germline activation, seminal fluid transfer, and male pheromone-mediated toxicity. Next, we summarize the current knowledge of genetic pathways involved in regulating mating-induced death, including DAF-9/DAF-12 steroid signaling, Insulin/IGF-1 signaling (IIS), and TOR signaling. Finally, we discuss the possible fitness benefits of mating-induced death. Throughout this review, we compare and contrast mating-induced death between the sexes and among different species in an effort to discuss this phenomenon and underlying mechanisms from the evolutionary perspective. Further investigation using mated C. elegans will improve our understanding of sexual antagonism, as well as the coordination between reproduction and somatic longevity in response to various external signals. Due to the evolutionary conservation in many aspects of mating-induced death, what we learn from a short-lived mated worm could provide new strategies to improve our own fitness and longevity.

Testosterone regulates CYP2J19-linked carotenoid signal expression in male red-backed fairywrens (Malurus melanocephalus).

Carotenoid pigments produce most red, orange and yellow colours in vertebrates. This coloration can serve as an honest signal of quality that mediates social and mating interactions, but our understanding of the underlying mechanisms that control carotenoid signal production, including how different physiological pathways interact to shape and maintain these signals, remains incomplete. We investigated the role of testosterone in mediating gene expression associated with a red plumage sexual signal in red-backed fairywrens (Malurus melanocephalus). In this species, males within a single population can flexibly produce either red/black nuptial plumage or female-like brown plumage. Combining correlational analyses with a field-based testosterone implant experiment and quantitative polymerase chain reaction, we show that testosterone mediates expression of carotenoid-based plumage in part by regulating expression of CYP2J19, a ketolase gene associated with ketocarotenoid metabolism and pigmentation in birds. This is, to our knowledge, the first time that hormonal regulation of a specific genetic locus has been linked to carotenoid production in a natural context, revealing how endocrine mechanisms produce sexual signals that shape reproductive success.

Jealousy Incarnate: Quiet Ego, Competitive Desire, and the Fictional Intelligence of Long-Term Mating in a Romantic K-Drama

In this paper, we analyze a K-drama aired by the Korean TV network SBS in 2016, Jealousy Incarnate, as a case study of the application of the Tie-Up Theory to a romantic narrative as a form of simulation of human mating processes with social cognition valence. We find that this case provides us with an example of a mating process where the choice of the male partner by the female lead character does not privilege the one that should be preferable on the basis of the standard prediction of the experimental research on human mating. This discrepancy is a signal of a basic limitation of experimental research, that highlights the subjects’ preferences for abstract potential partners but is not able to fully account for the mechanisms that lead to the choice of a specific partner in a specific mating interaction. We argue that the narrative simulation viewpoint provides insights that are complementary to those of experimental research, and that a more comprehensive theoretical approach, such as the one offered by the Tie-Up Theory, may be helpful to account for both perspectives.

Heterospecific mating interactions as an interface between ecology and evolution.

Reproductive interference (costly interspecific sexual interactions) is well-understood to promote divergence in mating-relevant traits (i.e. reproductive character displacement: RCD), but it can also reduce population growth, eventually leading to local extinction of one of the species. The ecological and evolutionary processes driven by reproductive interference can interact with each other. These interactions are likely to influence whether the outcome is coexistence or extinction, but remain little studied. In this paper, we first develop an eco-evolutionary perspective on reproductive interference by integrating ecological and evolutionary processes in a common framework. We also present a simple model to demonstrate the eco-evolutionary dynamics of reproductive interference. We then identify a number of factors that are likely to influence the relative likelihoods of extinction or RCD. We discuss particularly relevant factors by classifying them into four categories: the nature of the traits responding to selection, the mechanisms determining the expression of these traits, mechanisms of reproductive interference and the ecological background. We highlight previously underappreciated ways in which these factors may influence the relative likelihoods of RCD and local extinction. By doing so, we also identify questions and future directions that will increase our holistic understanding of the outcomes of reproductive interference.

Wasteful carotenoid coloration and its effects on territorial behavior in a cichlid fish

The famously diverse body coloration of cichlid fish serves communicative functions in mating and social interactions including competition for resources. Here, we examined the effects of a color pattern trait—the width of a yellow bar on a black body—on territorial competition in males and females of a color variant (“Ikola”) of the Lake Tanganyika cichlid Tropheus. First, measuring integumentary carotenoid concentrations in the yellow and black body regions, we established that wider yellow bars require more carotenoids allocated to body coloration. However, we also detected high carotenoid concentrations in the black body regions (> 100 µg/g fresh skin), raising questions about the function of non-displayed integumentary carotenoids. Behavioral experiments showed that fish with wider bars were quicker to explore an unfamiliar area of the tank. In experiments including presentations of fish dummies, the bar width of ‘territorial’ dummies had no effect on the latency time which test fish took to intrude into the dummies’ territories. However, male test fish performed fewer aggressive acts against wide-barred than against narrow-barred dummy competitors. Our results suggest that intimidation by wide bars as well as correlations between bar width and explorative behavior may contribute to mediating success in territorial Tropheus “Ikola”.

The ecological stage changes benefits of mate choice and drives preference divergence.

Preference divergence is thought to contribute to reproductive isolation. Ecology can alter the way selection acts on female preferences, making them most likely to diverge when ecological conditions vary among populations. We present a novel mechanism for ecologically dependent sexual selection, termed 'the ecological stage' to highlight its ecological dependence. Our hypothesized mechanism emphasizes that males and females interact over mating in a specific ecological context, and different ecological conditions change the costs and benefits of mating interactions, selecting for different preferences in distinct environments and different male traits, especially when traits are condition dependent. We test key predictions of this mechanism in a sympatric three-spine stickleback species pair. We used a maternal half-sib split-clutch design for both species, mating females to attractive and unattractive males and raising progeny on alternate diets that mimic the specialized diets of the species in nature. We estimated the benefits of mate choice for an indicator trait (male nuptial colour) by measuring many fitness components across the lifetimes of both sons and daughters from these crosses. We analysed fitness data using a combination of aster and mixed models. We found that many benefits of mating with high-colour males depended on both species and diet. These results support the ecological stage hypothesis for sticklebacks. Finally, we discuss the potential role of this mechanism for other taxa and highlight its ability to enhance reproductive isolation as speciation proceeds, thus facilitating the evolution of strong reproductive isolation. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Disentangling female postmating responses induced by semen transfer components in a simultaneous hermaphrodite

Optimizing reproductive success is an essential part of evolution for both sexes. Females can optimize mating by avoiding superfluous mating advances and insemination, since both take time away from other activities and may incur costs related to sperm receipt. While many separate-sexed organisms are known to exhibit mate avoidance, much less is known about this for simultaneous hermaphrodites. We addressed this here, using a simultaneously hermaphroditic species that can choose to mate in either of the two sex roles during each mating interaction. Recently, avoidance behaviours in response to natural matings were observed in the hermaphroditic pond snail Lymnaea stagnalis, potentially deterring insemination. To disentangle whether such behaviours are mediated by the mechanical act of mating or the receipt of accessory gland proteins and/or sperm, we intravaginally injected individuals with control or test fluids. Our results show that the avoidance behaviours, crawl-out and biting, were more frequently expressed when individuals were inseminated with accessory gland proteins and/or sperm. These behavioural components of the recipient increased time in courtship prior to insemination, which is concordant with the hypothesis that the partner tries to discourage the potential sperm donor from inseminating. Understanding the mechanism underlying the effects that molluscan accessory gland proteins induce contributes to our understanding of the molecular basis of the recipient's (behavioural) responses as well as how such biochemical postcopulatory strategies evolve.

Mating in the absence of fertilization promotes a growth-reproduction versus lifespan trade-off in female mice

Trade-offs between growth, reproduction, and lifespan constrain animal life histories, leading to evolutionary diversification of life history cycles in different environments. In female mammals, gestation and lactation are expected to impose the major costs of reproduction, driving reproductive trade-offs, although mating also requires interactions with males that could themselves influence life history. Here we show that a male's presence by itself leads to lifelong alterations in life history in female mice. Housing C57BL/6J female mice with sterilized males early in life led to an increase in body weight, an effect that persisted across life even when females were later allowed to produce pups. We found that those females previously housed with sterile males also showed enhanced late-life offspring production when allowed to reproduce, indicating that earlier mating can influence subsequent fecundity. This effect was the opposite to that seen in females previously housed with intact males, which showed the expected trade-off between early-life and late-life reproduction. However, housing with a sterile male early in life came at a cost to lifespan, which was observed in the absence of females ever undergoing fertilization. Endocrinologically, mating also permanently reduced the concentration of circulating prolactin, a pituitary hormone influencing maternal care. Changes in hormone axes that influence reproduction could therefore help alter life history allocation in response to opposite-sex stimuli. Our results demonstrate that mating itself can increase growth and subsequent fecundity in mammals, and that responses to sexual stimuli could account for some lifespan trade-offs normally attributed to pregnancy and lactation.

Temperature‐related breakdowns in the coordination of mating in Enchenopa binotata treehoppers (Hemiptera: Membracidae)

AbstractTemperature influences the expression of a wide range of behavioral traits in ectotherms, including many involved in the initiation of pair formation and mating. Although opportunities to mate are thought to be greatest when male and female activity overlap, sex‐specific behaviors and physiology could result in mismatched thermal optima for male and female courtship. Here, we investigate how conflicts in the thermal sensitivity of male and female courtship activity affect patterns of mating across temperatures in Enchenopa binotata treehoppers (Hemiptera: Membracidae). These plant‐feeding insects coordinate mating with plant‐borne vibrational signals exchanged in male–female duets prior to pair formation. We manipulated temperature across an ecologically relevant range (18–36ºC) and tested the likelihood of individual male and female E. binotata to engage in courtship activity using vibrational playbacks. We then staged male–female mating interactions across the same temperature range and quantified the thermal sensitivity of mating‐related behaviors across stages of mating. Specifically, we measured the timing of duetting, the likelihood for key pre‐copulatory behaviors to occur, whether the pair mated, and copulation duration. We found sex‐specific thermal sensitivity in courtship activity: Males showed a clear peak of activity at intermediate temperatures (27–30ºC), while females showed highest activity at the hotter thermal extreme. Mating rates, courtship duets, and copulatory attempts were less likely to occur at thermal extremes. Also, duetting occurred earlier and copulation was shortest at higher temperatures. Overall, our data suggest that sexes differ in how temperature affects mating‐related activity and some processes involved in mate coordination may be more sensitive than others across variable thermal environments.

Evidence for male genitalia detachment and female mate choice in the Australian stingless bee Tetragonula carbonaria

Mating systems are poorly understood for the majority of the world’s estimated 600 stingless bee species (Meliponini). It is assumed that in most species, a virgin queen takes a single nuptial flight, mates with a single drone and returns to the nest, using the stored sperm from this one event for the remainder of her life. Multiple genetic studies focused on stingless bee species from around the world have supported the hypothesis of single mating—monandry—by demonstrating shared paternity of workers within colonies. One possible mechanism for monandry is through male genitalia detachment during mating, which forms a residual mating plug inside the queen. Despite being thought to be the norm for stingless bees, male genitalia detachment has only been observed in a small number of species from the neotropics. Here I report on detailed observations of mating interactions for four queens of the Australian stingless bee Tetragonula carbonaria. Male genitalia detachment was observed in each case of copulation, providing the first evidence of male genitalia detachment in any Asian–Australian stingless bee lineage. Observations of the behaviour of queens also provide possible evidence for female mate choice in T. carbonaria. To more fully understand the mating system of T. carbonaria, further observations must be made of wild, natural copulation events, and the behaviour of the queen and the workers within the nest upon her return from the nuptial flight.

Versatility in a loud call: Dual affiliative and agonistic functions in the blue monkey boom

AbstractTo investigate the selective agents that shape signals, we examined function (adaptive benefit to signaler) in the boom loud call by male blue monkeys. Using natural observation and playbacks in a wild population in Kenya, we characterized boom function from conspecifics' behavioral responses and also variation in call usage relating to context and reproductive season. Booms occurred in several contexts and after varied stimuli, including falling branches, yet were strongly associated with intragroup activity and, in particular, affiliative interactions between callers and females. Males produced more booms during the mating season and, congruently, when more females in their groups were sexually active. After hearing booms, compared to no call, females spent more time near groupmates and the caller and were more likely to approach and have mating interactions with him. Males tended to move away after hearing a boom. In the aggregate, results indicate that booms achieve multiple functions relating to facilitating group cohesion, affiliative interactions, and mating opportunities, while also repelling rival males. An observed association with falling branches is puzzlingly distinct from these social functions. We explore the hypothesis that booms enable affiliative encounters by acting as signals of benign intent, and discuss the functional versatility of signals perceived by multiple receivers that vary in age, sex, and relationship to signalers.

Dynamic phenotypic correlates of social status and mating effort in male and female red junglefowl, Gallus gallus.

Despite widespread evidence that mating and intrasexual competition are costly, relatively little is known about how these costs dynamically change male and female phenotypes. Here, we test multiple hypotheses addressing this question in replicate flocks of red junglefowl (Gallus gallus). First, we test the interrelationships between social status, comb size (a fleshy ornament) and body mass at the onset of a mating trial. While comb size covaried positively with body mass across individuals of both sexes, comb size was positively related to social status in females but not in males. Second, we test for changes within individuals in body mass and comb size throughout the mating trial. Both body mass and comb size declined at the end of a trial in both sexes, suggesting that mating effort and exposure to the opposite sex are generally costly. Males lost more body mass if they (a) were socially subordinate, (b) were chased by other males or (c) mated frequently, indicating that subordinate status and mating are independently costly. Conversely, females lost more body mass if they were exposed to a higher frequency of coerced matings, suggesting costs associated with male sexual harassment and female resistance, although costs of mating per se could not be completely ruled out. Neither competitive nor mating interactions predicted comb size change in either sex. Collectively, these results support the notion that sex‐specific costs associated with social status and mating effort result in differential, sex‐specific dynamics of phenotypic change.

Sound production in the coconut crab, the largest terrestrial crustacean

Sound production in terrestrial crustaceans, including the coconut crab, Birgus latro, is not fully understood. Here, we present the first description of the acoustic features and sound production mechanisms of coconut crabs. The sound production system was determined based on X-ray videography and anatomical observations. The results indicated that the crabs produced a tapping sound by beating the scaphognathite, which is also used for ventilation, in the efferent branchial channel. The frequencies of the produced sounds were diverse, and the sound interval also varied within the same individual. From observations under captivity, differences in the sounds were confirmed at each mating phase. Although the relationship between the sounds and actions was not clarified in this study, it is probable that the crabs deliberately produce various types of sounds for different occasions. The coconut crab is known to use visual and chemical communication mechanisms, but these results suggest that a diverse set of sounds is an additional communication pathway during agonistic and mating interactions.

Dynamic networks of fighting and mating in a wild cricket population

Reproductive success is often highly skewed in animal populations. Yet the processes leading to this are not always clear. Similarly, connections in animal social networks are often nonrandomly distributed, with some individuals with many connections and others with few, yet whether there are simple explanations for this pattern has not been determined. Numerous social interactions involve dyads embedded within a wider network. As a result, it may be possible to model which individuals accumulate social interactions through a more general understanding of the social network's structure, and how this structure changes over time. We analysed fighting and mating interactions across the breeding season in a population of wild field crickets under surveillance from a network of video cameras. We fitted stochastic actor-oriented models to determine the dynamic process by which networks of cricket fighting and mating interactions form, and how they co-influence each other. We found crickets tended to fight those in close spatial proximity to them and those possessing a mutual connection in the fighting network, and heavier crickets fought more often. We also found that crickets that mated with many others tended to fight less in the following time period. This demonstrates that a mixture of spatial constraints, characteristics of individuals and characteristics of the immediate social environment are key for determining social interactions. The mating interaction network required very few parameters to understand its growth and thus its structure; only homophily by mating success was required to simulate the skew of mating interactions seen in this population. This demonstrates that relatively simple, but dynamic, processes can give highly skewed distributions of mating success. • Social network connections and patterns of mating success are both strongly skewed. • We modelled dynamic social (fighting) and mating networks in wild crickets. • The fighting network was influenced by proximity, sex, mass and mutual connections. • Only positive assortment by mating success was required to model the mating network. • In many populations, simple, dynamic processes may explain strong skews in fitness.