Mating Encounters Research Articles

Reproductive diapause influences spermatogenesis and testes’ size in the diplochronous wolf spider Allocosa senex (Lycosidae, Araneae) – A case study using a non-experimental approach

Seasonality considerably impacts on the life of organisms and leads to numerous evolutionary adaptations. Some species face seasonal changes by entering a diapause during different life stages. During adulthood, a diapause in the non-reproductive period can affect male gametogenesis as, for example, it occurs in insects. Spiders are distributed worldwide and show a variety of life cycles. However, data on spiders’ life cycles and seasonal adaptations are limited. Here, we explored the effect of reproductive diapause in a seasonal spider for the first time. We used the South American sand-dwelling spider Allocosa senex as a model as this species is diplochronous, meaning that individuals live two reproductive seasons, with juveniles and adults overwintering in burrows. It has been observed that individuals of this species reduce their metabolism during the non-reproductive season, diminishing prey consumption and locomotion to a minimum. This species is also well-known for exhibiting wandering and courting females and sedentary males. We analyzed spermatogenesis throughout the male's life cycle and described the male's reproductive system and spermiogenesis using light and transmission electron microscopy. We found that spermatogenesis in A. senex is asynchronous and continuous. However, when males face the non-reproductive season, the late spermatogenic stages and spermatozoa decline, causing an interruption but not a total arrest of this process. This seasonality is also reflected in smaller testes’ size in males from the non-reproductive season than in other periods. The mechanisms and constraints are unknown, but they could be related to the metabolic depression during this life cycle period. Since sex-role reversal apparently sets a low-intensity sperm competition scenario compared with other wolf spiders, surviving two reproductive seasons may balance mating opportunities by distributing them between both periods. Thus, the partial interruption of spermatogenesis during diapause could allow new mating encounters during the second reproductive season.

Aerial Drones Reveal the Dynamic Structuring of Sea Turtle Breeding Aggregations and Minimum Survey Effort Required to Capture Climatic and Sex-Specific Effects

Quantifying how animals use key habitats and resources for their survival allows managers to optimise conservation planning; however, obtaining representative sample sizes of wildlife distributions in both time and space is challenging, particularly in the marine environment. Here, we used unoccupied aircraft systems (UASs) to evaluate temporal and spatial variation in the distribution of loggerhead sea turtles (Caretta caretta) at two high-density breeding aggregations in the Mediterranean, and the effect of varying sample size and survey frequency. In May–June of 2017 to 2019, we conducted 69 surveys, assimilating 10,075 inwater turtle records at the two sites. Optimal time interval between surveys to capture the dynamics of aggregations over the breeding period was <2-week intervals and >500 turtles (from the combined surveys). This minimum threshold was attributed to the core-area use of female turtles shifting across surveys in relation to wind direction to access warmer nearshore waters and male presence. Males were more widely distributed within aggregations than females, particularly in May when mating encounters were high. Most males were recorded swimming and oriented parallel to shore, likely to enhance encounter rates with females. In contrast, most females were generally stationary (resting on the seabed or basking), likely to conserve energy for reproduction, with orientation appearing to shift in relation to male numbers at the breeding area. Thus, by identifying the main factors regulating the movement and distribution of animals, appropriate survey intervals can be selected for appropriate home range analyses. Our study demonstrates the versatility of UASs to capture the fine-scale dynamics of wildlife aggregations and associated factors, which is important for implementing effective conservation.

Learning to anticipate mate presence shapes individual sex roles in the hermaphroditic pond snail, Lymnaea stagnalis

Despite being simultaneously male and female, hermaphrodites may still need to assume the male or female sexual role in a mating encounter, with the option to swap roles afterwards. For the great pond snail, Lymnaea stagnalis, deciding which sexual role to perform has important consequences, since sperm transfer and male reproductive success can be decreased. We hypothesised that detecting cues that indicate a possible mating encounter could help them to adapt their mating behaviour. Therefore, we experimentally assessed whether signalling the presence of a conspecific with an odour can affect the sexual role of Lymnaea stagnalis. The results showed that learning resulted in either an increased ability to mate as a male or in faster mating compared to the control group. These findings reveal that learning shapes the mating dynamics of Lymnaea stagnalis, thus showing that cognitive processes not only affect mating in separate-sexed species but also in hermaphrodites.

Interactions With Plant Defences Isolate Sympatric Populations of an Herbivorous Mite

Host plant specialisation can promote evolutionary divergence between herbivore populations associated with different plant species. While the mechanisms by which specialist species exploit their hosts have been studied widely across taxa, less is known about the mechanisms that allow intraspecific variants to arise and to be maintained across spatial and temporal scales. To understand whether adaptations to plant defences against herbivory contribute to the co-existence of genetically distinct populations of an herbivore, we investigate the interaction between honeysuckle (Lonicera periclymenum) and sympatric specialist and generalist populations of the spider miteTetranychus urticae. We found that mite folivory induces the production of sticky droplets on honeysuckle, which have a defensive role: they increase mite mortality directly, and potentially indirectly by increasing the arrestment of a predator. We show that droplet induction and the preference to feed on honeysuckle depend on mite genotype, where the generalist avoids this host and the specialist suppresses droplet production. These traits are heritable and dominant in F1 hybrids between generalists and specialists. Selection pressure from honeysuckle and differences in host preference likely reduce the opportunity of mating encounters on this host. We propose that the interplay between selection from host plant defences and ecological barriers to hybridisation contribute to the persistence of genetically distinct populations of a single species in sympatry.

Outcomes of previous mating encounters influence mate preferences and memory in meadow voles, Microtus pennsylvanicus

Animals use social information to select and modify mate preferences. Future mate choice decisions for previous partners may depend on the outcomes of their mating interactions. Using meadow voles, Microtus pennsylvanicus , we investigated whether their preference for the location of a previous mating encounter would be maintained or modified depending on the outcome of the mating encounter. We conducted preference tests in a T-maze before and after subjects were paired. First, the subjects were allowed to choose between two potential mates and were then paired with their preferred individual for 4 h. They were then returned to an empty T-maze 6 days (males) and 21 days (males and females) following the paired encounter and allowed to explore, during which we recorded the time that individuals spent investigating each section of the maze that previously contained the partner and alternative conspecifics. The outcome of the mating encounters did not cause males to maintain or modify their preference for the location of their partners, 6 days later. Likewise, males and females did not maintain or modify their preferences for the location of their partners, 21 days later, if a barrier prevented them from mating and if they made no mating attempt. This was also exhibited among female subjects whose partners attempted to mate. However, 21 days later (the length of gestation for females), males that successfully mated or attempted to mate maintained their preference for the location of their mate, while females that mated either maintained or modified their preference for the location of their mate depending on whether they produced pups. These results suggest that meadow voles use the information they gain from previous interactions to guide their future mate preferences. Their ability to recall the location of successful mating encounters may be a way to increase their overall fitness. • Mate preferences depend on the outcomes of previous interactions in meadow voles. • Male meadow voles may be able to predict when a female will be in postpartum oestrus. • Prior mating success with individuals influences future mate choice decisions. • Meadow voles have the potential to recall the location of previous mates.

Solifuge (camel spider) reproductive biology: an untapped taxon for exploring sexual selection

The exploration of new and diverse animal groups in the study of sexual selection is both necessary and important to help better understand broad patterns and test sexual selection hypotheses regarding the evolutionary origins and maintenance of reproductive tactics and associated traits. Solifuges are, in this matter, an exceptional group and very little explored from the sexual selection point of view. At first glance, mating is apparently quite simple and conserved within this arachnid order, but solifuge reproductive behavior is unique among arachnids and more diverse than previously thought. In particular, these voracious animals appear to exhibit high sexual conflict, as males need to avoid being eaten by their aggressive female partners and mating encounters in some species involve periods of apparently male-induced female inactivity during sperm transfer. The extent to which reproductive encounters are coercive versus collaborative, however, remains largely unknown. In this review, we begin with a historical perspective of sexual behavior research in solifuges. We then discuss precopulatory mating patterns, the role of the female and male during mating, sexual dimorphism, and the influence of sexual selection during different stages of mating. In addition, we explore cases of sexual cannibalism and provide an updated analysis of how postcopulatory sexual selection may be acting on these amazing arachnids. This review shows that there is much to be done in this extraordinary group of animals.

Termite males enhance mating encounters by changing speed according to density.

Search theory predicts that animals evolve efficient movement patterns to enhance encounter rates with specific targets. The optimal movements vary with the surrounding environments, which may explain the observation that animals often switch their movement patterns depending on conditions. However, the effectiveness of behavioural change during search is rarely evaluated because it is difficult to examine the actual encounter dynamics. Here we studied how partner-seeking termites update their search strategies depending on the local densities of potential mates. After a dispersal flight, termites drop their wings and walk to search for a mate; when a female and a male meet, they form a female-led tandem pair and search for a favourable nesting site. If a pair is separated, they have two search options-reunite with their stray partner, or seek a new partner. We hypothesized that the density of individuals affects separation-reunion dynamics and thus the optimal search strategy. We observed the searching process across different densities and found that termite pairs were often separated but obtained a new partner quickly at high mate density. After separation, while females consistently slowed down, males increased their speed according to the density. Under high mate density, separated males obtained a partner earlier than females, who do not change movement with density. Our data-based simulations confirmed that the observed behavioural change by males contributes to enhancing encounters. Males at very low mate densities did best to move slowly and thereby reduce the risk of missing their stray partner, who is the only available mate. On the other hand, males that experienced high mate densities did better in mating encounters by moving fast because the risk of isolation is low, and they must compete with other males to find a partner. These results demonstrate that termite males adaptively update their search strategy depending on conditions. Understanding the encounter dynamics experienced by animals is key to connecting the empirical work to the idealized search processes of theoretical studies.

Mating behaviour of Eremobates pallipes (Say, 1823) (Arachnida: Solifugae: Eremobatidae)

Little is known about the reproductive behaviour of solifuges, or camel spiders (Arachnida: Solifugae). Behavioural research is limited, due in part to challenges of maintaining specimens in the laboratory where they can be best observed. The present study documents the courtship and mating behaviours of a North American solifuge, Eremobates pallipes (Say, 1823) through staged mating encounters in an arena within a laboratory setting. Trials were filmed and analysed to establish sequence and timing of behaviours. We were able to document consistent and predictable aspects of the mating behaviours in this species. The consistent use by males of the suctorial organs during mating was documented for the first time in Eremobatidae.

Ratiometric GPCR signaling enables directional sensing in yeast.

Accurate detection of extracellular chemical gradients is essential for many cellular behaviors. Gradient sensing is challenging for small cells, which can experience little difference in ligand concentrations on the up-gradient and down-gradient sides of the cell. Nevertheless, the tiny cells of the yeast Saccharomyces cerevisiae reliably decode gradients of extracellular pheromones to find their mates. By imaging the behavior of polarity factors and pheromone receptors, we quantified the accuracy of initial polarization during mating encounters. We found that cells bias the orientation of initial polarity up-gradient, even though they have unevenly distributed receptors. Uneven receptor density means that the gradient of ligand-bound receptors does not accurately reflect the external pheromone gradient. Nevertheless, yeast cells appear to avoid being misled by responding to the fraction of occupied receptors rather than simply the concentration of ligand-bound receptors. Such ratiometric sensing also serves to amplify the gradient of active G protein. However, this process is quite error-prone, and initial errors are corrected during a subsequent indecisive phase in which polarity clusters exhibit erratic mobile behavior.

Opportunity for female choice in the wild is frequently curtailed by low male trait variation in Hyla versicolor

To understand the efficacy of female choice in driving the evolution of male displays, we need to not only characterize preferences but examine the opportunity for the expression of such preferences. Mate assessment by females should be constrained if the relative attractiveness of multiple displays is perceived as equal because trait differences between them are indistinguishable. This is expected to result in apparently arbitrary mate choice, and knowledge about the frequency of such mating patterns is crucial in predicting the strength of sexual selection. Here, we examine discrimination abilities of female Hyla versicolor in the context of actual male-male chorus variation. We found that roughly half of mating encounters in the wild do not provide the call variation required for the expression of female preferences (non-arbitrary choice). Interestingly, the trait for which female H. versicolor shows the strongest preference during playback trials (call duration) is not the trait whose difference will most often be detectable to females in the wild (call rate). Furthermore, we document individual variation in discrimination ability, with some females being able to discriminate multiple traits, while others only focus on one trait. This suggests that the relatively high estimate of arbitrary mating is not only due to females struggling to discriminate natural local variation overall but due to an abundance of individuals with limited discrimination abilities that require encounters with males that differ in the specific trait they will discriminate. Lastly, small trait differences between males do not arise from nearest neighbors plastically altering their calls to be more similar. These findings provide insights on the frequently observed mismatch between laboratory phonotaxis and actual mating success in the wild. How and why animals choose a mate are complicated questions. For many species (like the gray treefrog), we have good descriptions of the male advertisement and the female preferences. However, much less is known about the actual expression of such preferences in the wild, which rests on the opportunity for females to encounter perceptible variation among males. We determined the minimum acoustic differences necessary for females to detect a “more attractive” call and compared those abilities to male-male variation in the chorus. We predict that a female will encounter sufficiently disparate calls only half of the time, with all other choice events appearing to be arbitrary decisions (both calls sound equally attractive). This abundance of arbitrary mating is driven not only by low variation among males but also by wide disparity in discrimination abilities of females. These findings may explain why we often observe unexpectedly unpredictable mating patterns in other taxa.

Me against who? Male guppies adjust mating behaviour according to their rival’s presence and attractiveness

AbstractSexual selection theory suggests that males need to constantly reappraise their mating decisions to take account of the presence and the phenotypes of their rivals. Here we examine this expectation by asking: (i) If the presence of a rival influences male mating behaviour; (ii) How important is the attractiveness of the rival (absolute attractiveness) in shaping male behaviour; and (iii) How does a male's attractiveness in comparison to his rival (relative attractiveness) influence a male's mating decisions. Using the Trinidadian guppy, a species in which female mate choice (based on males’ attractive traits) plays an important role in male mating outcomes, we recorded the frequency of courtship displays and unsolicited attempts by focal males. First, we quantified focal male mating behaviour with and without a rival. Since the probability of a successful mating is, on average, halved by the presence of a rival, we predicted that under competition the focal male would invest more in less costly mating tactic—unsolicited attempts. Second, we examined how the rival's standard length and area of orange coloration mediated focal male mating behaviour. We found that rival presence influenced how focal males responded to females in terms of both mating tactics. However, the rival attractiveness elicited changes only in male courtship display. Focal males increased courtship display rate if his rival was small or if possessed large amounts of orange, regardless of considering rival absolute or relative attractiveness. Our results show that males invest in the costlier mating tactic when there is no rival or in the presence of a smaller rival. Interestingly, they make a similar investment in the presence of an attractive orange rival. Overall, this study highlights the importance of fine‐grained male decisions in mating encounters and shows that mating tactics are differentially shaped by multiple competition risk cues.

Sexually differential movements and optimization of mating encounters

Sexually differential movements and optimization of mating encounters

Opportunities for female choice in the bed bug Cimex lectularius

AbstractBed bugs are cited as exemplars of sexual conflict because mating can only occur via traumatic insemination. However, past antagonistic coevolution between the sexes does not necessarily preclude current female choice. Here, we investigate opportunities for precopulatory female choice in bed bugs. We examined whether females seek out mating opportunities when they gain the most benefit: when females are virgin and/or have recently fed. But, we found that female mating and feeding status had little effect on female attraction to males and male odor. To determine whether females approach male harborages (home crevices) to seek matings in nature, we investigated where matings occurred among unfamiliar pairs of bed bugs. We found that, despite female attraction to male odor, matings were most likely to take place in the female's harborage rather than the male's harborage. We also examined the effect of feeding on male and female ability to mate. Whereas previous research reported that engorgement impaired female ability to refuse matings, we found that male feeding status had a larger effect on the success of mating encounters than female feeding status. Fed males had poor mating success, suggesting that males may be faced with a trade‐off between mating and feeding.

Sexually experienced, but not naïve, female rats show a conditioned object preference (COP) for mating after a single training trial

Female rats with mating experience spend more time with the male rat, exhibit shorter contact-return latency to intromission, and display more proceptive behaviors in the male rat's compartment than during the first mating experience. The present study tested 1) whether mating induced conditioned object preference (COP) is possible with a single conditioning trial and 2) whether a preference is induced for an object associated with the first mating encounter or the fifth mating encounter in female rats. Ovariectomized, Long-Evans female rats were primed with estradiol benzoate + progesterone and either exposed to an empty paced mating chamber for 15 min (Naïve) or received a 15 intromission test of paced mating behavior (Experienced) on four separate occasions before undergoing the COP procedure. Experienced, but not Naïve, female rats developed a COP for a single mating bout, indicating that mating is highly rewarding for sexually experienced female rats. The findings raise questions about the effect of sexual experience on reward regions in the brain, the responsiveness of genital tissue, and learning mechanisms.

Assessment of Maturity in the Eastern Gulf of Mexico Florida Stone Crab Menippe mercenaria Fishery

AbstractThe Florida stone crab Menippe mercenaria supports one of Florida's most valuable commercial fisheries. Sustained fishing pressure and overexploitation, despite negative trends in landings, have facilitated the need to transition from stock assessments based on effort and landings toward more sophisticated methods. This requires accurate knowledge of life history parameters, such as size at sexual maturity. The physiological, behavioral, and functional maturity of female Florida stone crabs and the physiological maturity of male crabs were assessed in individuals collected throughout the geographically fished range of the population between 2013 and 2014. Morphological maturity of both sexes was assessed in individuals collected from the same locations in 2005–2016. Histology was used to determine oocyte maturity, presence of spermatophores, and presence of postovulatory follicles in females and the production of spermatophores (present in the anterior vas deferens) in males. Decision tree analysis determined that 50% of females were mature at 43 mm carapace width (CW) based on an indicator of physiological and behavioral sexual maturity. In males, physiological maturity occurred at a CW of 34.75 mm. Sexual maturity estimated using morphological maturity occurred at 66.3 mm CW in females and 63.1 mm CW in males. Differences in estimated size at sexual maturity between morphological maturity and physiological, behavioral, and functional maturity indicate that the relative growth of body parts is not reliable for estimating sexual maturity in Florida stone crabs. Smaller females may be contributing more to the spawning population than had been previously estimated. Large, morphometrically mature males may be more successful in mating encounters, but during times of flux in population size structure (i.e., fewer large males), morphologically immature but physiologically mature males have increased mating opportunities. Results indicate that male and female Florida stone crabs can contribute to the reproductive population multiple times before they become vulnerable to the fishery.

One and Done: Long-Term Sperm Storage in the Cactus-Feeding Bug, Narnia femorata (Hemiptera: Coreidae)

Female sperm storage is common across a wide taxonomic range. The temporal separation of mating and fertilization has several benefits for females. It enables sperm selection from multiple males, but can also allow females to temporally and spatially delay fertilization until the proper environmental conditions are found. In this study, we investigated the extent and possible function of sperm storage in the polygamous cactus-feeding bug, Narnia femorata Stal (Hemiptera: Coreidae). To determine the viability of stored sperm over time, we tracked life-long fecundity of females exposed to varying levels of male access. We exposed females to four treatments: one male for 1 wk, one male for 1 wk with further exposure to the same male later in her life for an additional week, one male for the duration of her life, or two males (subsequent) for the duration of her life. Our results indicate that females can store sperm and produce viable offspring during their lifespan from a relatively brief mating encounter with a single male. Furthermore, egg production and fertility rates did not differ across treatments, suggesting that time of exposure to mates and number of mates (monandry vs. polyandry) has no effect on N. femorata fecundity. Sperm storage seems to operate independently of mate number or availability, and is therefore, likely an adaptation to the patchy spatial-temporal distribution of adequate resources.

Ejaculation Induced by the Activation of Crz Neurons Is Rewarding to Drosophila Males

The reward system is a collection of circuits that reinforce behaviors necessary for survival [1, 2]. Given the importance of reproduction for survival, actions that promote successful mating induce pleasurable feeling and are positively reinforced [3, 4]. This principle is conserved in Drosophila, where successful copulation is naturally rewarding to male flies, induces long-term appetitive memories [5], increases brain levels of neuropeptide F (NPF, the fly homolog of neuropeptide Y), and prevents ethanol, known otherwise as rewarding to flies [6, 7], from being rewarding [5]. It is not clear which of the multiple sensory and motor responses performed during mating induces perception of reward. Sexual interactions with female flies that do not reach copulation are not sufficient to reduce ethanol consumption [5], suggesting that only successful mating encounters are rewarding. Here, we uncoupled the initial steps of mating from its final steps and tested the ability of ejaculation to mimic the rewarding value of full copulation. We induced ejaculation by activating neurons that express the neuropeptide corazonin (CRZ) [8] and subsequently measured different aspects of reward. We show that activating Crz-expressing neurons is rewarding to male flies, as they choose to reside in a zone that triggers optogenetic stimulation of Crz neurons and display conditioned preference for an odor paired with the activation. Reminiscent of successful mating, repeated activation of Crz neurons increases npf levels and reduces ethanol consumption. Our results demonstrate that ejaculation stimulated by Crz/Crz-receptor signaling serves as an essential part of the mating reward mechanism in Drosophila. VIDEO ABSTRACT.

The optimal movement patterns for mating encounters with sexually asymmetric detection ranges

Animals have evolved various sex-specific characteristics to improve the efficiency of mating encounters. One is the sex-specific attracting signal. Signal receivers perform a combination of random search and navigation before and after signal detections. On the other hand, signal senders can also modify their movement patterns to optimize their encounter rates, which invokes a reverse side of random search problems that asks for the most efficient movement patterns of signal senders to be found by signal receivers. In this study, we focused on visual and auditory signals in particular, and quantified the efficiency of mating encounters of individual animals performing a Lévy walk, a special class of random walk, with a variety of speeds before signal detection. We found that signal senders should move more slowly and/or less diffusively than receivers to improve mating encounters. The optimal movement patterns of senders ranged from relatively slow to stationary ones depending on the density of individuals, the effective range of signals, and the ability of receivers to locate senders. By focusing on the optimal movement patterns of individuals that are often assumed to be given targets, the present study provides insights into strategies of effective attraction beyond the case of mate search.

Neurogenesis in the olfactory bulb induced by paced mating in the female rat is opioid dependent.

The possibility to control the rate of sexual stimulation that the female rat receives during a mating encounter (pacing) increases the number of newborn neurons that reach the granular layer of the accessory olfactory bulb (AOB). If females mate repeatedly, the increase in the number of neurons is observed in other regions of the AOB and in the main olfactory bulb (MOB). It has also been shown that paced mating induces a reward state mediated by opioids. There is also evidence that opioids modulate neurogenesis. In the present study, we evaluated whether the opioid receptor antagonist naloxone (NX) could reduce the increase in neurogenesis in the AOB induced by paced mating. Ovariectomized female rats were randomly divided in 5 different groups: 1) Control (not mated) treated with saline, 2) control (not mated) treated with naloxone, 3) females that mated without controlling the sexual interaction (no-pacing), 4) females injected with saline before pacing the sexual interaction and 5) females injected with NX before a paced mating session. We found, as previously described, that paced mating induced a higher number of new cells in the granular layer of the AOB. The administration of NX before paced mating, blocked the increase in the number of newborn cells and prevented these cells from differentiating into neurons. These data suggest that opioid peptides play a fundamental role in the neurogenesis induced by paced mating in female rats.

Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles.

Summary paragraphAdult pair bonding involves dramatic changes in the perception and valuation of another individual1. One key change is that partners come to reliably activate the brain's reward system2-6, though the precise neural mechanisms by which partners become rewarding during sociosexual interactions leading to a bond remain unclear. Using a prairie vole model of social bonding7, we show how a functional circuit from medial prefrontal cortex (mPFC) to nucleus accumbens (NAcc) is dynamically modulated to enhance females' affiliative behavior towards a partner. Individual variation in the strength of this functional connectivity, particularly after the first mating encounter, predicts how quickly animals begin affiliative huddling with their partner. Rhythmically activating this circuit in a social context without mating biases later preference towards a partner, indicating that this circuit's activity is not just correlated with how quickly animals become affiliative but causally accelerates it. These results provide the first dynamic view of corticostriatal activity during bond formation, revealing how social interactions can recruit brain reward systems to drive changes in affiliative behavior.