Neural Circuits of Sexual Behavior in Caenorhabditis elegans.

The recently determined connectome of the Caenorhabditis elegans adult male, together with the known connectome of the hermaphrodite, opens up the possibility for a comprehensive description of sexual dimorphism in this species and the identification and study of the neural circuits underlying sexual behaviors. The C. elegans nervous system consists of 294 neurons shared by both sexes plus neurons unique to each sex, 8 in the hermaphrodite and 91 in the male. The sex-specific neurons are well integrated within the remainder of the nervous system; in the male, 16% of the input to the shared component comes from male-specific neurons. Although sex-specific neurons are involved primarily, but not exclusively, in controlling sex-unique behavior-egg-laying in the hermaphrodite and copulation in the male-these neurons act together with shared neurons to make navigational choices that optimize reproductive success. Sex differences in general behaviors are underlain by considerable dimorphism within the shared component of the nervous system itself, including dimorphism in synaptic connectivity.

It's about Her: Male Within-Season Movements Are Related to Mate Searching in a Songbird.

AbstractIn species with resource-defense mating systems (such as most temperate-breeding songbirds), male dispersal is often considered to be limited in both frequency and spatial extent. When dispersal occurs within a breeding season, the favored explanation is ecological resource tracking. In contrast, movements of male birds associated with temporary emigration, such as polyterritoriality (i.e., defense of an additional location after attracting a female in the initial territory), are usually attributed to mate searching. We suggest that male dispersal and polyterritoriality are functionally related and that mate searching may be a unifying hypothesis for predicting the within-season movements of male songbirds. Here, we test three key predictions derived from this hypothesis in Wood Warblers (Phylloscopus sibilatrix). We collected data on the spatial behavior of 107 males between 2017 and 2019 and related male movements to a new territory (in both a dispersal and a polyterritorial context) to mating potential in the current territory. Most males dispersed from their territories within days or weeks after failing to attract a female, despite occupying territories in apparently suitable habitat. Probability of polyterritoriality by paired males increased after the peak fertile period of their mate. Males never dispersed following nest predation if the female remained to renest. Thus, our data are consistent with the hypothesis that both movement types are functionally related to mate searching.

When Synchrony Makes the Best of Both Worlds Even Better: How Well Do We Really Understand Facultative Sex?

Biological diversity abounds in potential study topics. Studies of model systems have their advantages, but reliance on a few well-understood cases may create false impressions of what biological phenomena are the norm. Here I focus on facultative sex, which is often hailed as offering the best of both worlds, in that rare sex offers benefits almost equal to obligate sex and avoids paying most of the demographic costs. How well do we understand when and why this form of sexual reproduction is expected to prevail? I show several gaps in the theoretical literature and, by contrasting asynchronous with synchronous sex, highlight the need to link sex theories to the theoretical underpinnings of bet hedging, on the one hand, and to mate limitation considerations, on the other. Condition-dependent sex and links between sex with dispersal or dormancy appear understudied. While simplifications are justifiable as a simple assumption structure enhances analytical tractability, much remains to be done to incorporate key features of real sex to the main theoretical edifice.

Mate-searching context of prey influences the predator-prey space race.

Predation risk is a strong driver of prey distribution and movement. However, fitness-influencing behaviours, such as mating, can alter risk and influence predator-prey space-use dynamics. In tree crickets, Oecanthus henryi, mate searching involves acoustic signalling by immobile males and phonotactic movement by females. Space-use patterns in tree crickets relative to their primary predators, green lynx spiders (Peucetia viridans), should therefore depend on their current mate-searching state; whether males are calling or non-calling and whether females are phonotactic or non-phonotactic. We first measured the degree of spatial anchoring of crickets to specific bushes in the field and determined whether that influenced the probability of broad-scale spatial overlap with spiders. In the absence of spiders, all crickets, independent of sex or male calling status, were found to be spatially anchored to specific types of bushes and not uniformly distributed on the landscape. At the broad spatial scale, spiders were more likely to be found on bushes with female crickets and, to a lesser degree, calling male crickets. At a finer spatial scale within a bush, movement strategies of crickets not only varied depending on the presence or absence of a spider, but also on their current mate-searching state. Phonotactic females showed clear predator avoidance, whereas calling and non-calling males moved towards the spider instead of away, similar to predator inspection behaviour seen in many taxa. As the strongly selected sex, males are more likely to undertake risky mate-searching activities, which includes inspection of predator positions. Overall, we found that all crickets were predictably anchored at the landscape scale, but their sex and mate-seeking behaviour influenced the degree of overlap with predators and their antipredator movement strategies. Reproductive strategies within a prey species, therefore, can alter predator-prey space race at multiple spatial scales.

Male black widows parasitize mate-searching effort of rivals to find females faster.

Mate-searching success is a critical precursor to mating, but there is a dearth of research on traits and tactics that confer a competitive advantage in finding potential mates. Theory and available empirical evidence suggest that males locate mates using mate-attraction signals produced by receptive females (personal information) and avoid inadvertently produced cues from rival males (social information) that indicate a female has probably already mated. Here, we show that western black widow males use both kinds of information to find females efficiently, parasitizing the searching effort of rivals in a way that guarantees competition over mating after reaching a female's web. This tactic may be adaptive because female receptivity is transient, and we show that (i) mate searching is risky (88% mortality) and (ii) a strongly male-biased operational sex ratio (from 1.2 : 1 to more than 10 : 1) makes competition inevitable. Males with access to rivals' silk trails moved at higher speeds than those with only personal information, and located females even when personal information was unreliable or absent. We show that following rivals can increase the potential for sexual selection on females as well as males and argue it may be more widespread in nature than is currently realized.

Sex differences in pollinator behavior: Patterns across species and consequences for the mutualism.

Intraspecific variation in floral visitor behaviour and pollination efficiency has been much less studied than interspecific variation. Nevertheless, it is clear that large differences in these traits exist within species, and in particular between sexes within species. With the exception of a few well-studied interactions, however, the consequences of these differences in the pollinators and visited plants remain to be investigated. In this review, we document large and consistent differences in the foraging patterns of male and female pollinators that have been demonstrated to directly affect plant reproduction or that have clear potential to do so. Males and females differ in visitation frequency, type of flowers visited, and per-visit pollen transfer. Females gather more and different resources from flowers compared to males, and males generally tend to show more mobile foraging patterns than females. We argue that these sex-associated patterns have broad generality across pollinators, and that sex-associated differences can in some cases be larger than differences between species. We offer predictions about how these patterns will influence pollinator preference, specialization, and fidelity, as well as the cost, quality and quantity of pollination service to plants. In the face of increasing threats to plant-pollinator interactions, understanding their basic functioning and the variation inherent in their component parts is critical. We advocate for more attention to sex-based differences among pollinators in particular, and the consequences of intraspecific variation more broadly.

Male behavioural plasticity depends on maternal mating status in the two-spotted spider mite.

In haplodiploid organisms including the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), both unmated and mated females can produce male offspring. A previous study reported that males produced by unmated females (UM males) find pre-reproductive females more quickly than males produced by mated females (M males) in T. urticae. However, it remains unclear what factors cause the difference. We investigated effects of maternal mating status on mate-searching behaviour of their sons by changing the sons' developmental environment. In T. urticae, the primary sex ratio of mated-female colonies is female-biased. For both UM and M males, half of individuals were reared with males to imitate unmated-female colonies, whereas the rest were reared with females to imitate mated-female colonies. In UM males, individuals that had developed with males found pre-reproductive females more quickly than those that had developed with females. However, such a difference was not observed in M males. This indicates that behavioural response to the developmental environment differs between UM and M males. It means that the behavioural plasticity depends on maternal mating status. When males were individually reared, however, there was no significant difference in the mate-searching behaviour between UM and M males, indicating that maternal mating status does not independently affect their sons' mate-searching behaviour. This study showed that male mate-searching behaviour is changed by their developmental environment and maternal mating status. This behavioural plasticity depending on maternal mating status is the first reported in haplodiploid organisms.

Exploratory decisions of the Caenorhabditis elegans male: a conflict of two drives.

The ability to generate behavioral plasticity according to ever-changing physiological demands and environmental conditions is a universal feature of decision-making circuits in all animals. Decision-making requires complex integration of internal states with sensory context. As a mate searching strategy, the Caenorhabditis elegans male modifies his exploratory behavior in relation to a source of food according to recent sensory experience with mates. Information about the reproductive and nutritional status of the male is also incorporated in his choice of exploratory behavior. The study of mate searching in the C. elegans male, a genetic model organism with a nervous system of only 383 neurons, provides the opportunity to elucidate the molecular and cellular mechanisms of state-dependent control of behavior and sensory integration. Here I review our progress in understanding the physiological and environmental regulation of the male's exploratory choices - to explore in search of mates or to exploit a source of food - and the neural circuits and neuromodulator pathways underlying this decision.

The effect of sex-biased dispersal on opposite-sexed spatial genetic structure and inbreeding risk.

Natal sex-biased dispersal has long been thought to reduce the risk of inbreeding by spatially separating opposite-sexed kin. Yet, comprehensive and quantitative evaluations of this hypothesis are lacking. In this study, we quantified the effectiveness of sex-biased dispersal as an inbreeding avoidance strategy by combining spatially explicit simulations and empirical data. We quantified the extent of kin clustering by measuring the degree of spatial autocorrelation among opposite-sexed individuals (FM structure). This allowed us to systematically explore how the extent of sex-biased dispersal, generational overlap, and mate searching distance, influenced both kin clustering, and the resulting inbreeding in the absence of complementary inbreeding avoidance strategies. Simulations revealed that when sex-biased dispersal was limited, positive FM genetic structure developed quickly and increased as the mate searching distance decreased or as generational overlap increased. Interestingly, complete long-range sex-biased dispersal did not prevent the development of FM genetic structure when generations overlapped. We found a very strong correlation between FM genetic structure and both FIS under random mating, and pedigree-based measures of inbreeding. Thus, we show that the detection of FM genetic structure can be a strong indicator of inbreeding risk. Empirical data for two species with different life history strategies yielded patterns congruent with our simulations. Our study illustrates a new application of spatial genetic autocorrelation analysis that offers a framework for quantifying the risk of inbreeding that is easily extendable to other species. Furthermore, our findings provide other researchers with a context for interpreting observed patterns of opposite-sexed spatial genetic structure.

Mate finding, Allee effects and selection for sex-biased dispersal.

Although dispersal requires context-dependent decision-making in three distinct stages (emigration, transit, immigration), these decisions are commonly ignored in simple models of dispersal. For sexually reproducing organisms, mate availability is an important factor in dispersal decisions. Difficulty finding mates can lead to an Allee effect where population growth decreases at low densities. Surprisingly, theoretical studies on mate finding and on sex-biased dispersal produce opposing predictions: in the former, one sex is predicted to move less if the other sex evolves to search more, whereas in the latter, mate-finding difficulties can select for less sex bias in dispersal when mate finding occurs after dispersal. Here, we develop a pair of models to examine the joint evolution of dispersal and settlement behaviour. Our first model resolves the apparent contradiction from the mate search and dispersal literatures. Our second model demonstrates that the relationship between mating system and sex-biased dispersal is more complex than a simple contrast between resource defence monogamy and female defence polygyny. Our results highlight that a key factor is the timing of mating relative to dispersal (before, during, or after). We also show that although movement has the potential to alleviate a mate-finding Allee effect, in some cases, it can actually exacerbate the effect.

Mate sampling and choosiness in the sand goby.

To date, mate choice studies have mostly focused on establishing which mates are chosen or how the choices are performed. Here, we combined these two approaches by empirically testing how latency to mate is affected by various search costs, variation in mate quality and female quality in the sand goby (Pomatoschistus minutus). Our results show that females adjust their mating behaviour according to the costs and benefits of the choice situation. Specifically, they mated sooner when access to males was delayed and when the presence of other females presented a mate sampling cost. We also found a positive link between size variation among potential mating partners and spawning delay in some (but not all) experimental conditions. By contrast, we did not find the number of available males or the females' own body size ('quality') to affect mating latency. Finally, female mating behaviour varied significantly between years. These findings are notable for demonstrating that (i) mate sampling time is particularly sensitive to costs and, to a lesser degree, to variation among mate candidates, (ii) females' mating behaviour is sensitive to qualitative rather than to quantitative variation in their environment, and (iii) a snapshot view may describe mate sampling behaviour unreliably.

Sexual dimorphism in aipysurine sea snakes (Elapidae, Hydrophiinae).

The transition from terrestrial to aquatic life by hydrophiine elapid snakes modified targets of natural selection and likely affected sexual selection also. Thus, the shift to marine life also might have affected sexual dimorphism. Our measurements of 419 preserved specimens of six species of aipysurine snakes (genera Emydocephalus and Aipysurus) revealed sexual dimorphism in mean adult snout-vent length (SVL), body width relative to SVL, lengths and widths of heads and tails relative to SVL, and eye diameter relative to head length. Females averaged larger than males in all taxa, and generally were wider-bodied with shorter and wider tails and smaller eyes. For other traits, sexual dimorphism varied among species: for example, relative head length ranged from male-biased to female-biased, and head shape (width relative to length) was highly dimorphic only in A. laevis. The transition to marine life may have eliminated male-male combat (reducing selection for large males) and favoured visual rather than pheromone-based mate-searching (favouring larger eyes in males). Variation in head-size dimorphism may reflect intersexual niche partitioning, with different taxa following different trajectories. Repeated evolutionary transitions from terrestrial to aquatic life in snakes provide a powerful opportunity to explore selective forces on sexually dimorphic traits.

Body stiffness is a mechanical property that facilitates contact-mediated mate recognition in Caenorhabditis elegans.

Physical contact is prevalent in the animal kingdom to recognize suitable mates by decoding information about sex, species, and maturity. Although chemical cues for mate recognition have been extensively studied, the role of mechanical cues remains elusive. Here, we show that C. elegans males recognize conspecific and reproductive mates through short-range cues, and that the attractiveness of potential mates depends on the sex and developmental stages of the hypodermis. We find that a particular group of cuticular collagens is required for mate attractiveness. These collagens maintain body stiffness to sustain mate attractiveness but do not affect the surface properties that evoke the initial step of mate recognition, suggesting that males utilize multiple sensory mechanisms to recognize suitable mates. Manipulations of body stiffness via physical interventions, chemical treatments, and 3D-printed bionic worms indicate that body stiffness is a mechanical property for mate recognition and increases mating efficiency. Our study thus extends the repertoire of sensory cues of mate recognition in C. elegans and provides a paradigm to study the important roles of mechanosensory cues in social behaviors.

Changes in the activity budget of the fiddler crab Leptuca uruguayensis throughout the reproductive period in temperate estuaries.

Animal reproductive success implies the performance of several behaviours, such as courting, mate searching, copulation, offspring production and care. These behaviours usually have high energetic and ecological costs. Therefore, to maximise their reproductive success, animals should make choices throughout their lives, such as deciding how much energy to invest in different activities, according to their conditions and needs. In temperate estuaries, the fiddler crab L. uruguayensis has a short reproductive period, with two synchronous spawning events. Considering that reproductive behaviours incur high energetic cost to fiddler crabs, we estimated how this species manages its activity budget throughout the reproductive period, to quantify trade-offs between the time spent on reproductive behaviours versus time spent on other activities. By analysing videos of females and males recorded in the field at different moments of the reproductive period, we observed that pre-copulatory behaviours, such as female wandering and male waving were more intense at the beginning of the reproductive period, suggesting that most matings occurred before the first spawning event but not before the second one. The ecological conditions during the breeding season and the individual strategies adopted by males and females mostly determine when and how much time to spend on courtship behaviours, and behavioural plasticity can be expected whenever the conditions change. The strategy used by L. uruguayensis for energy management, females' ability to store male gametes and environmental temperatures might have been the main factors determining the relative time spent in courtship behaviours during the reproductive period.

Intersexual Differences in Behaviour and Resource Use of Specialist Phengaris teleius Butterflies.

Although the behaviour of the Large Blue butterflies of the genus Phengaris (= Maculinea) is relatively well studied, most empirical data come from investigations of their dispersal and oviposition. Here, we assessed overall intersexual differences in resource use by tracking Phengaris teleius (Bergsträsser, 1779) individuals and recording the duration of their behaviours. Females were characterised by frequent, short flights, and devoted more time to resting and oviposition. Males engaged in numerous, but usually short interactions, and spent most of the time in flight exploring their surroundings for receptive females. Their average flight time was significantly longer compared to females. Average feeding time did not differ between the sexes but was shorter when butterflies were feeding on Sanguisorba officinalis L. Intraspecific interactions within P. teleius were three times longer than those with other insect species, and interactions between sexes were particularly long lasting. Significantly shorter interspecific interactions imply that butterflies can easily recognise conspecifics and differentiate between sexes, which offers obvious fitness benefits. Both sexes, but especially females, showed strong association with their larval host plant, and less so with other flowers of similar colour and shape. Females predominantly used their host plant for feeding, which possibly indicates neuro-sensory constraints towards this resource.

Males, but not females, perform strategic mate searching movements between host plants in a leaf beetle with scramble competition polygyny.

Mate searching is assumed to be performed mostly by males, but when females benefit from multiple mating or are under risk of failing to mate, they may also perform mate searching. This is especially important in scramble competition polygynies, in which mate searching is the main mechanism of mate competition. Typically, more mobile individuals are expected to achieve higher mating success because mobility increases their probability of finding mates. If we assume individual movements are mainly explained by mate searching in scramble competition polygynies, we can investigate searching strategies by asking when individuals should leave their location and where they should go. We hypothesize that individuals will leave their locations when mating opportunities are scarce and will seek spatially close sites with better mating opportunities. We tested these hypotheses for males and females of Leptinotarsa undecimlineata, a leaf beetle with scramble competition polygyny in which both sexes are promiscuous. Individuals mate and feed exclusively on Solanum plants, and thus, individual movements can be described as switches between plants. Females were less likely than males to leave isolated plants, and both males and females moved preferentially to neighboring plants. Males were more likely to leave when the local number of females was low, and the number of males was high. They moved to plants with more females, a behavior consistent with a mate searching strategy. Females were more likely to move to plants with fewer males and many females, a behavior consistent with male harassment avoidance. Strategic movement is widely considered in foraging context, but seldom in a mate searching context. Considering that selection to minimize searching costs, maximize mating success, and minimize harassment may be ubiquitous in nature, we argue that strategic movements by mate searching individuals are likely to occur in many species.

To forage, mate, or thermoregulate: Influence of resource manipulation on male rattlesnake behavior.

Male animals should preferentially allocate their time to performing activities that promote enhancing reproductive opportunity, but the need to acquire resources for growth and survival may compete with those behaviors in the short term. Thus, behaviors which require differing movement patterns such as ambushing prey and actively searching for mates can be mutually exclusive. Consequently, males that succeed at foraging could invest greater time and energy into mate searching. We radio-tracked sixteen male massasauga rattlesnakes (Sistrurus catenatus) and supplemented the diets of half the snakes with mice across an active season. We tested the predictions that reduced foraging needs would allow fed snakes to move (i.e., mate search) more, but that they would consequently be stationary to thermoregulate less, than unfed controls. Contrary to our first prediction, we found no evidence that fed snakes altered their mate searching behavior compared to controls. However, we found controls maintained higher body temperatures than fed snakes during the breeding season, perhaps because fed snakes spent less time in exposed ambush sites. Fed snakes had higher body condition scores than controls when the breeding season ended. Our results suggest the potential costs incurred by devoting time to stationary foraging may be outweighed by the drive to increase mating opportunities. Such instances may be especially valuable for massasaugas and other temperate reptiles that can remain inactive for upwards of half their lives or longer in some cases, and for female rattlesnakes that generally exhibit biennial or more protracted reproductive cycles.

Not what it looks like: mate-searching behaviour, mate preferences and clutch production in wandering and territory-holding female fiddler crabs.

Risks inherent in mate-searching have led to the assumption that females moving sequentially through populations of courting males are sexually receptive, but this may not be true. We examined two types of fiddler crab females: wanderers moving through the population of courting males and residents that were occupying and defending their own territories. Sometimes residents leave territories to look for new burrows and we simulated this by displacing wanderers and residents and observing their behaviour while wandering. We predicted that the displaced wanderers would exhibit more mate-searching behaviours than resident females. However, wandering and resident females behaved nearly identically, displaying mate-searching behaviours and demonstrating matching mate preferences. Also, males behaved the same way towards both female types and similar proportions of wanderers and residents stayed in a male's burrow to mate. But more wanderers than residents produced egg clutches when choosing a burrow containing a male, suggesting females should be categorized as receptive and non-receptive. Visiting and rejecting several males is not the defining feature of female mate choice. Moving across the mudflat by approaching and leaving a succession of burrows (mostly occupied by males) is an adaptive anti-predator behaviour that is useful in the contexts of mate-searching and territory-searching.