Mating Opportunities Research Articles

Coevolutionary maintenance of forked tails and song in hirundines (Aves: Hirundininae)

Both conspicuous plumage ornamentation and song are well‐known examples of sexually selected traits, but their interrelationship is not well known, perhaps in part because of confounding factors, including interspecific variation in ecology, habitat, morphology, and type of ornamentation. Here, using a phylogenetic comparative approach and the 69 species with available information (i.e. 96% of all 72 species), I examined the evolutionary relationship between forked tails and the presence/absence of song in hirundines (Aves: Hirundininae). Hirundines have similar ecology (e.g. aerial insectivores, social monogamy, and biparental provisioning), morphology (e.g. syrinx with nearly complete bronchial rings), and plumage ornamentation (i.e. a sexually selected forked tail), which provides a unique opportunity to examine the evolutionary associations between plumage ornamentation and song. In particular, hirundines have repeatedly lost their ornamentation, forked tails, setting up a condition to test their association with the evolutionary gain/loss of their simple song. After controlling for phylogeny and covariates, I demonstrated that song was less likely to be found in species with forkless tails than in species with forked tails. Two correlates of tail shape, sexual dimorphism in the overall plumage characteristics as a well‐known proxy of sexual selection and incubation type as a measure of extrapair mating opportunity, were not positively related to the presence or absence of song, indicating the importance of forked tails, rather than their correlates. The analysis of the correlated evolution of discrete characters further supported the correlated evolution of the two traits, in which forked tails and song are maintained together and less likely to be lost under the presence of each other. The current study provided macroevolutionary support for the integrated use of visual and acoustic courtship traits.

Warmer springs increase potential for temporal reproductive isolation among habitat patches in subalpine flowering plants

Abstract Flowering phenology can vary considerably even at fine spatial scales, potentially leading to temporal reproductive isolation among habitat patches. Climate change could alter flowering synchrony, and hence temporal isolation, if plants in different microhabitats vary in their phenological response to climate change. Despite the importance of temporal isolation in determining patterns of gene flow, and hence population genetic structure and local adaptation, little is known about how changes in climate affect temporal isolation within populations. Here, we use flowering phenology and floral abundance data of 50 subalpine plant species over 44 years to test whether temporal isolation between habitat patches is affected by spring temperature. For each species and year, we analysed temporal separation in peak flowering and flowering overlap between habitat patches separated by 5–950 m. Across our study species, warmer springs were associated with more temporal differentiation in flowering peaks among habitat patches, and less flowering overlap, increasing potential for temporal isolation within populations. Synthesis. By reducing opportunities for mating among plants in nearby habitat patches, our results suggest that warmer springs may reduce opportunities for gene flow within populations, and, consequently, the capacity of plant populations to adapt to environmental changes.

Trade-offs between immunity and competitive ability in fighting ant males

BackgroundFighting disease while fighting rivals exposes males to constraints and trade-offs during male-male competition. We here tested how both the stage and intensity of infection with the fungal pathogen Metarhizium robertsii interfere with fighting success in Cardiocondyla obscurior ant males. Males of this species have evolved long lifespans during which they can gain many matings with the young queens of the colony, if successful in male-male competition. Since male fights occur inside the colony, the outcome of male-male competition can further be biased by interference of the colony’s worker force.ResultsWe found that severe, but not yet mild, infection strongly impaired male fighting success. In late-stage infection, this could be attributed to worker aggression directed towards the infected rather than the healthy male and an already very high male morbidity even in the absence of fighting. Shortly after pathogen exposure, however, male mortality was particularly increased during combat. Since these males mounted a strong immune response, their reduced fighting success suggests a trade-off between immune investment and competitive ability already early in the infection. Even if the males themselves showed no difference in the number of attacks they raised against their healthy rivals across infection stages and levels, severely infected males were thus losing in male-male competition from an early stage of infection on.ConclusionsMales of the ant C. obscurior have a well-developed immune system that raises a strong immune response very fast after fungal exposure. This allows them to cope with mild pathogen exposures without compromising their success in male-male competition, and hence to gain multiple mating opportunities with the emerging virgin queens of the colony. Under severe infection, however, they are weak fighters and rarely survive a combat already at early infection when raising an immune response, as well as at progressed infection, when they are morbid and preferentially targeted by worker aggression. Workers thereby remove males that pose a future disease threat by biasing male-male competition. Our study thus reveals a novel social immunity mechanism how social insect workers protect the colony against disease risk.

Light disrupts social memory via a retina-to-supraoptic nucleus circuit.

The formation of social memory between individuals of the opposite sex is crucial for expanding mating options or establishing monogamous pair bonding. A specialized neuronal circuit that regulates social memory could enhance an individual's mating opportunities and provide a parallel pathway for computing social behaviors. While the influence of light exposure on various forms of memory, such as fear and object memory, has been studied, its modulation of social recognition memory remains unclear. Here, we demonstrate that acute exposure to light impairs social recognition memory (SRM) in mice. Unlike sound and touch stimuli, light inhibits oxytocin neurons in the supraoptic nucleus (SON) via M1 SON-projecting intrinsically photosensitive retinal ganglion cells (ipRGCs) and GABAergic neurons in the perinuclear zone of the SON (pSON). We further show that optogenetic activation of SON oxytocin neurons using channelrhodopsin is sufficient to enhance SRM performance, even under light conditions. Our findings unveil a dedicated neuronal circuit through which luminance affects SRM, utilizing a non-image-forming visual pathway, distinct from the canonical modulatory role of the oxytocin system.

X chromosome drive is constrained by sexual selection and influences ornament evolution.

Experimental evolution provides an integrative method for revealing complex interactions among evolutionary processes. One such interaction involves sex-linked selfish genetic elements and sexual selection. X-linked segregation distorters, a type of selfish genetic element, influence sperm transmission to increase in frequency and consequently alter the population sex ratio and the opportunity for sexual selection, while sexual selection may impact the spread of X-linked distorters. Here we manipulated sexual selection by controlling female mating opportunities and the presence of a distorting X chromosome in experimental lines of the stalk-eyed fly, Teleopsis dalmanni, over 11 generations. We find that removal of sexual selection leads to an increase in the frequency of the X-linked distorter and sex ratio across generations and that post-copulatory sexual selection alone is sufficient to limit the frequency of distorters. In addition, we find that male eyestalk length, a trait under pre-copulatory sexual selection, evolves in response to changes in the strength of sexual selection with the magnitude of the response dependent on X chromosome type and the frequency of distorting X chromosomes. These results reveal how a selfish X can interact with sexual selection to influence the evolution of sexually selected traits in multiple ways.

Group size and mating system predict sex differences in vocal fundamental frequency in anthropoid primates

Vocalizations differ substantially between the sexes in many primates, and low-frequency male vocalizations may be favored by sexual selection because they intimidate rivals and/or attract mates. Sexual dimorphism in fundamental frequency may be more pronounced in species with more intense male mating competition and in those with large group size, where social knowledge is limited and efficient judgment of potential mates and competitors is crucial. These non-mutually exclusive explanations have not been tested simultaneously across primate species. In a sample of vocalizations (n = 1914 recordings) across 37 anthropoid species, we investigated whether fundamental frequency dimorphism evolved in association with increased intensity of mating competition (H1), large group size (H2), multilevel social organization (H3), a trade-off against the intensity of sperm competition (H4), and/or poor acoustic habitats (H5), controlling for phylogeny and body size dimorphism. We show that fundamental frequency dimorphism increased in evolutionary transitions towards larger group size and polygyny. Findings suggest that low-frequency male vocalizations in primates may have been driven by selection to win mating opportunities by avoiding costly fights and may be more important in larger groups, where limited social knowledge affords advantages to rapid assessment of status and threat potential via conspicuous secondary sexual characteristics.

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.

Influence of Nutritional Stress on Female Allocation and Somatic Growth in the Simultaneously Hermaphroditic Polychaete Worm Ophryotrocha diadema.

Hermaphrodites are characterized by plastic sex allocation, by which they adjust their allocation of reproductive resources according to mating opportunities. However, since the plasticity of sex allocation is influenced by environmental conditions, it may also be affected by species-specific life-history traits. In this study, we explored the trade-off between nutritional stress due to food deficiency and the investment of resources in female allocation and somatic growth in the simultaneously hermaphroditic polychaete worm, Ophryotrocha diadema. To achieve this, we exposed adult individuals to three food supply levels: (1) ad libitum-100% food supply, (2) intense food deficiency-25% food resources, and (3) extreme food deficiency-0% food resources. Our findings show a progressive decrease in female allocation in the numbers of cocoons and eggs and in body growth rate of O. diadema individuals as the level of nutritional stress increased.

Home Range and Habitat Use of Translocated Alligator Snapping Turtles (Macrochelys temminckii) in an Extensive River System

Macrochelys temminckii (Alligator Snapping Turtle) occurs at low densities in the Choctawhatchee River system in Florida. Translocation could help bolster the population, but its effectiveness for this species is not well studied. We released 9 adults into a cutoff of the Choctawhatchee River and radio-tracked them from Sept 2017 to May 2019 to monitor movements and habitat use. Turtles had significantly larger home-range distances than previously reported (12,882.8 ± 8781.5 m for males and 10,621.6 ± 6020.4 m for females), but all established a home range overlapping with 1 or more individuals. On several occasions turtles were found together, suggesting interaction and potential mating opportunities. This study suggests that translocation may be an effective strategy for augmenting populations of this species.

Age-specific survival of territorial and non-territorial male chamois.

How alternative reproductive tactics (ARTs) are maintained in wildlife populations is one of the major questions in evolutionary biology. As a dominant status, territoriality is typically linked to increased mating opportunities, and one explanation why this behaviour coexists with other tactics is that dominance implies survival costs. Such a trade-off may occur in the Northern chamois Rupicapra rupicapra, as reproductive advantages of territorial males over non-territorial males could be counterbalanced by a reduction in survival mediated through energy expenditure, stress and parasitic infections, ultimately favouring ART coexistence. Here, we analysed age-dependent survival probabilities of territorial (n = 15) and non-territorial (n = 16) adult chamois using information collected over 12 years between 2010 and 2021 in the Gran Paradiso National Park (Western Italian Alps). Survival rates were estimated with a CMR approach using Burnham's joint modelling of live encounter and dead recovery data. The model selection procedure, based on AICc value minimisation, supported a linear decrease of survival with age but the results did not match our predictions, as territorial chamois did not have lower survival rates than non-territorial chamois. In contrast, territorial males appeared to enjoy reproductive success at lower survival costs. This, in turn, supports the role of other factors, such as snow-dependent environmental stochasticity, in the maintenance of ARTs in chamois populations. The limited sample size, however, calls for caution in interpretation, and long-term studies of lifetime reproductive success and survival are necessary to clarify the mechanisms underlying the expression and coexistence of different reproductive behaviours in this species.

Tradeoffs between mating effort and parenting effort in a polygynandrous mammal

Reproductive strategies are defined by expenditures of time and energy devoted to mating effort, which increases mating opportunities, and parenting effort, which enhances the survival of offspring. We examine tradeoffs between mating effort and parenting effort in male olive baboons, Papio anubis, a species in which males compete for mating opportunities, but also form ties to lactating females (primary associations) that represent a form of parenting effort. Males that are involved in more primary associations invest less in mating effort than males who are involved in fewer primary associations. Males that are involved in more primary associations play a smaller role in establishing proximity to their primary associates than other males, suggesting that males operate under temporal constraints. There is also some evidence that involvement in primary associations negatively affects paternity success. Taken together, the data suggest that males face tradeoffs between mating effort and parenting effort.

Male attention allocation depends on social context

Allocation of attention, typically a limited capacity, is a mechanism used to filter large amounts of information and determine what stimuli are most relevant at a particular moment. In dynamic social environments as found in almost all species, including humans, multiple individuals may play a pivotal role in any given interaction where a male’s attention may be divided between a rival, a current mate, and/or future potential mates. Although clearly important, the role of the social environment on attention in animals is not well understood. Here, we investigated impacts of the social environment on attention allocation using male sailfin mollies, Poecilia latipinna, which are a part of a sexual-unisexual mating system with the Amazon molly, Poecilia formosa. We asked: 1) Does the species of female influence the amount of attention a male allocates to her? And 2) Is a male’s attention towards his mate influenced by different social partners? We show that males perceive a larger male as a more relevant stimulus to pay attention to compared to a smaller male, and a conspecific female (either a partner or audience) as a more relevant stimulus compared to a heterospecific female. Our results show that differential allocation of attention is dependent upon multiple components of the social environment in which an individual interacts. Understanding what qualities of rival males or potential mates provide enough meaning to males to cause a shift in attention away from a mating opportunity is essential to understanding the influence of the social environment in sexual selection.

Volatiles of fungal cultivars act as cues for host-selection in the fungus-farming ambrosia beetle Xylosandrus germanus.

Many wood-boring insects use aggregation pheromones during mass colonization of host trees. Bark beetles (Curculionidae: Scolytinae) are a model system, but much less is known about the role of semiochemicals during host selection by ambrosia beetles. As an ecological clade within the bark beetles, ambrosia beetles are obligately dependent on fungal mutualists for their sole source of nutrition. Mass colonization of trees growing in horticultural settings by exotic ambrosia beetles can occur, but aggregation cues have remained enigmatic. To elucidate this mechanism, we first characterized the fungal associates of the exotic, mass-aggregating ambrosia beetle Xylosandrus germanus in Southern Germany. Still-air olfactometer bioassays documented the attraction of X. germanus to its primary nutritional mutualist Ambrosiella grosmanniae and to a lesser extent another common fungal isolate (Acremonium sp.). During two-choice bioassays, X. germanus was preferentially attracted to branch sections (i.e., bolts) that were either pre-colonized by conspecifics or pre-inoculated with A. grosmanniae. Subsequent analyses identified microbial volatile organic compounds (MVOCs) that could potentially function as aggregation pheromones for X. germanus. To our knowledge, this is the first evidence for fungal volatiles as attractive cues during host selection by X. germanus. Adaptive benefits of responding to fungal cues associated with an infestation of conspecifics could be a function of locating a suitable substrate for cultivating fungal symbionts and/or increasing the likelihood of mating opportunities with the flightless males. However, this requires solutions for evolutionary conflict arising due to potential mixing of vertically transmitted and horizontally acquired symbiont strains, which are discussed.

Fire effects on plant reproductive fitness vary among individuals, reflecting pollination-dependent mechanisms.

Fire induces flowering in many plant species worldwide, potentially improving reproductive fitness via greater availability of resources, as evident by flowering effort, and improved pollination outcomes, as evident by seed set. Postfire increases in flowering synchrony, and thus mating opportunities, may improve pollination. However, few studies evaluate fire effects on multiple components of fitness. Consequently, the magnitude and mechanism of fire effects on reproductive fitness remain unclear. Over multiple years and prescribed burns in a prairie preserve, we counted flowering stems, flowers, fruits, and seeds of three prairie perennials, Echinacea angustifolia, Liatris aspera, and Solidago speciosa. We used aster life-history models to assess how fire and mating opportunities influenced annual maternal fitness and its components in individual plants. In Echinacea and Liatris, but not in Solidago, fire increased head counts, and both fire and mating opportunities increased maternal fitness. Burned Echinacea and Liatris plants with many flower heads produced many seeds despite low seed set (fertilization rates). In contrast, plants with an average number of flower heads had high seed set and produced many seeds only when mating opportunities were abundant. Fire increased annual reproductive fitness via resource- and pollination-dependent mechanisms in Echinacea and Liatris but did not affect Solidago fitness. The consistent relationship between synchrony and seed set implies that temporal mating opportunities play an important role in pollination. While fire promotes flowering in many plant species, our results reveal that even closely related species exhibit differential responses to fire, which could impact the broader plant community.

Sex differences in the expression of aggressive behavior and influences on social choice in zebrafish (Danio rerio)

Aggregation behavior (grouping) provides many animals with the ecological benefits of protection from predators, increased access to food, and greater mating opportunities, despite possible costs. Many factors likely contribute to the social choices animals make, and we sought to determine if the individual expression of aggression would correlate with shoalmate choices. We quantified aggressive or submissive tendencies of individual male and female zebrafish and shoalmate preferences within dichotomous choice assays. We hypothesized that fish, regardless of their individual aggressive behaviors, would benefit most and therefore choose to spend time near larger shoals and shoals of the opposite sex. Both sexes spent significantly more time near shoals rather than be alone. Males spent significantly more time with the largest shoal, and females exhibited a similar trend. Both sexes spent more time with shoals of females, rather than males. Males were generally more consistent in their aggressive behaviors across multiple assays and females exhibited more individual-variability. More aggressive male zebrafish were more likely to choose shoals of males over females and were more likely to swim alone, but female zebrafish did not exhibit a correlation between aggressive behaviors and social choices. Our results demonstrate clear sex differences in the expression of individual behavior and influences on shoaling.

Mite dilemma: molting to acquire sexual maturity or not molting to ensure durability and dispersal ability in Phorytocarpais fimetorum (Parasitiformes; Gamasida; Parasitidae)

Dispersal from birthplace is an effective strategy to cope up with unpredictable environmental change. In many animals, dispersal is carried out prior to mating and reproduction to avoid inbreeding. However, this also means that the dispersers must find mates in the new habitat. Phorytocarpais fimetorum (= former name Parasitus fimetorum) is a free-living predatory mite inhabiting animal dung and manure. In such ephemeral habitats, the mites quickly develop from egg to deutonymph as the environmentally tolerant, dispersal stage via larva and protonymph stages. After dispersal to new habitats utilizing dung beetles as phoretic hosts, deutonymphs have to decide whether to molt to adulthood by losing their tolerance and migration ability or not to molt and continue dispersal. Here, using molt-suppressing deutonymphs that were obtained under isolated conditions, I investigated whether food conditions (amount of rearing medium bearing nematodes as prey) and encounters with conspecifics stimulate their molting. A drastic increase in food resources induced molting in both sexes, but the responses to the pairing treatment were different between sexes. Whereas female deutonymphs molted at the encounter with males regardless of whether they were deutonymphs or adults, molting of male deutonymphs was induced only at the pairing with female deutonymphs (not adult females). Because adult females are usually nonvirgin and have already started oviposition, the males seemed to discriminate against them. The decision about molting is understandable as a male mate choice, which is adaptive to the limited mating opportunities in ephemeral environments.

Androgen-armoured amazons: reversed sex roles in coucals are associated with testosterone in females but not males

In some species, sexual selection is stronger in females than males. In classically polyandrous birds, for instance, females compete for mating opportunities and males care for offspring. Sex steroids such as testosterone have been suggested to regulate the behaviours of 'role-reversed' females and males, but comparative studies did not find evidence for a role of testosterone in relation to sex roles. However, the large variability of hormone measurements across laboratories may prevent detecting subtle differences in hormone levels. To circumvent this caveat, I compared sex steroid concentrations of females and males of two closely related and cohabiting species with different mating systems: the classically polyandrous black coucal (Centropus grillii) and the monogamous white-browed coucal (C. superciliosus). Baseline and gonadotropin-releasing hormone (GnRH)-induced testosterone concentrations were twice as high in female black coucals than female white-browed coucals, and the low pre-breeding progesterone concentrations of female black coucals were consistent with progesterone's modulatory role during agonistic interactions in this species. Baseline and GnRH-induced testosterone and progesterone concentrations did not differ between males of both species. This study provides first evidence that elevated testosterone is associated with sex-role-reversed traits in females, whereas low levels of testosterone may not be necessary to facilitate sex-role reversal in males.

Social network differences and phenotypic divergence between stickleback ecotypes

Abstract Elucidating the mechanisms underlying differentiation between populations is essential to our understanding of ecological and evolutionary processes. While social network analysis has yielded numerous insights in behavioral ecology in recent years, it has rarely been applied to questions about population differentiation. Here, we use social network analysis to assess the potential role of social behavior in the recent divergence between two three-spined stickleback ecotypes, “whites” and “commons”. These ecotypes differ significantly in their social behavior and mating systems as adults, but it is unknown when or how differences in social behavior develop. We found that as juveniles, the white ecotype was bolder and more active than the common ecotype. Furthermore, while there was no evidence for assortative shoaling preferences, the two ecotypes differed in social network structure. Specifically, groups of the white ecotype had a lower clustering coefficient than groups of the common ecotype, suggesting that groups of the white ecotype were characterized by the formation of smaller subgroups, or “cliques”. Interestingly, ecotypic differences in the clustering coefficient were not apparent in mixed groups composed of whites and commons. The formation of cliques could contribute to population divergence by restricting the social environment that individuals experience, potentially influencing future mating opportunities and preferences. These findings highlight the insights that social network analysis can offer into our understanding of population divergence and reproductive isolation.

A Neural Circuit Controlling Virgin Female Aggression Induced by Mating-related Cues in Drosophila.

Females increase aggression for mating opportunities and for acquiring reproductive resources. Although the close relationship between female aggression and mating status is widely appreciated, whether and how female aggression is regulated by mating-related cues remains poorly understood. Here we report an interesting observation that Drosophila virgin females initiate high-frequency attacks toward mated females. We identify 11-cis-vaccenyl acetate (cVA), a male-derived pheromone transferred to females during mating, which promotes virgin female aggression. We subsequently reveal a cVA-responsive neural circuit consisting of four orders of neurons, including Or67d, DA1, aSP-g, and pC1 neurons, that mediate cVA-induced virgin female aggression. We also determine that aSP-g neurons release acetylcholine (ACh) to excite pC1 neurons via the nicotinic ACh receptor nAChRα7. Together, beyond revealing cVA as a mating-related inducer of virgin female aggression, our results identify a neural circuit linking the chemosensory perception of mating-related cues to aggressive behavior in Drosophila females.

Bidirectional sex change and plasticity of gonadal phases in the goby Lubricogobius exiguus.

Of the ca. 500 known hermaphroditic fish species, bidirectional sex change and simultaneous hermaphroditism are currently known in 69 and 57 species, respectively. Both bidirectional sex change and simultaneous hermaphroditism are predicted to evolve when mating opportunities are limited, such as in cases of low-density distribution and low mobility of individuals. However, the plasticity of sex is adaptive in obtaining mating opportunities, especially when there is mate loss. Pair-rearing experiments and histological observations of gonads of the goby Lubricogobius exiguus, which has low-density distributions and low mobility, showed bidirectional sex change. The male-role individuals in pairs had gonads in which only the testis was functional (male-phase), whereas the female-role individuals had two types of gonads: only the ovary was functional (female-phase) or both testis and ovary were functional (simultaneously hermaphroditic phase, SH-phase). In addition, single-rearing experiments showed SH-phase gonads in all individuals, and some cyclic spawning but no self-fertilization occurred. These results revealed that L. exiguus has an unusual sexual pattern among hermaphroditic fishes because they undergo bidirectional sex change and some maintain SH-phase gonads. These findings indicate that the low-density distribution and low mobility of L. exiguus in their natural habitat may have influenced the evolution of this unique sexual pattern.