Color polymorphism in the Cuban endemic livebearing fish Limia vittata (Teloestei, Poeciliidae): Potential roles of sexual and natural selection.

Color polymorphism can be maintained in natural populations by natural selection or sexual selection. In this study, we use two different approaches to test which of these evolutionary mechanisms may explain the presence of color polymorphism in the Cuban Limia (Limia vittata), an endemic livebearing fish from Cuba. First, we investigate the role of sexual selection using traditional binary choice tests looking at both female and male preferences relative to varying degrees of black spotting in stimulus mates. Second, we assess the role of natural selection by analyzing the frequency and geographic distribution of black-spotted and nonspotted morphs of L. vittata in natural populations from Cuba. The frequency of black-spotted morphs is significantly higher in brackish and saltwater environments compared with freshwater habitats, which could be related to higher predation pressure in coastal ecosystems compared with purely freshwater environments. Our results suggest that habitat variation is the most important factor in maintaining color polymorphism in L. vittata. Salinity levels could be indirectly responsible for maintaining different color morphs in this species, likely due to the regulatory effect of saline gradients on predation regimes.

Neural mechanisms involved in female mate choice in invertebrates.

Mate choice is a critical decision with direct implications for fitness. Although it has been recognized for over 150 years, our understanding of its underlying mechanisms is still limited. Most studies on mate choice focus on the evolutionary causes of behavior, with less attention given to the physiological and molecular mechanisms involved. This is especially true for invertebrates, where research on mate choice has largely focused on male behavior. This review summarizes the current state of knowledge on the neural, molecular and neurohormonal mechanisms of female choice in invertebrates, including behaviors before, during, and after copulation. We identify areas of research that have not been extensively explored in invertebrates, suggesting potential directions for future investigation. We hope that this review will stimulate further research in this area.

Thin-fingered fiddler crabs display a natural preference for UV light cues but show no sensory bias to other hypertrophied claw coloration.

Although color cues play an important role in sociosexual signaling, when communication is exploited as a foraging cue by predators, prey must pay the due cost for sustaining information interchange. In this regard, fiddler crabs draw attention by having flashy enlarged claws that could potentially attract the interest of many predators. Surprisingly, the adaptive function of claw coloration in fiddler crabs is not entirely understood and have barely been studied in American species. Here, we examine the spectral reflectance of thin-fingered (Leptuca leptodactyla) fiddler crabs' hypertrophied claws and evaluate whether female conspecifics prefer UV-light or other color cues. We test whether male claws reflect UV light and whether females use UV light and/or other color cues when making mating decisions. Our results reveal that only the most flamboyant enlarged claws should be detected by female conspecifics, which show a clear preference for male UV signals. Moreover, while the anterior portion of the enlarged claws (pointing towards conspecifics) reflect UV light, claws' dorsal portion and carapaces (which possibly point upwards and might attract airborne predators) do not show an UV peak. We also discuss the possibility of hypertrophied claws working as honest aposematic signals or playing an important role as decoys.

Finding love in a hopeless place: A global database of misdirected amplexus in anurans.

Amphibians are one of the most species-rich vertebrate taxa, with diverse and complex reproductive behaviors. Even though mate recognition plays a vital role in reproductive success, unusual amplexus with non-suitable mates (misdirected amplexus) have been reported to occur in the wild. Misdirected amplexus may decrease fitness, thus likely having ecological and evolutionary consequences and their frequency might increase with human-induced changes in habitat. However, it is still unclear what promotes this unusual behavior and how widespread it is at spatial and phylogenetic scales. To fill this gap, we compiled a global database of misdirected amplexus events from literature and personal observations, with detailed information on environmental, geographical, and behavioral aspects of reported events. Furthermore, we discuss its spatial, temporal, and phylogenetic patterns. We provide a data set of 378 misdirected amplexus events for 156 amplectant species distributed across 69 genera and 18 families distributed in 52 countries in all continents except Antarctica. We collected data published or collected during the last 100 years, from 1920 to 2020, with information on the hour, month, and year of the misdirected amplexus events. We recorded a total of 282 interspecific amplexus, 46 necrophiliac amplexus, and 50 amplexus with objects or non-amphibian species, with the United States and Brazil being the countries with the highest number of records. Misdirected amplexus did not occur equally in all zoogeographical realms, with most events occurring in the Neotropical and Nearctic realms. Interspecific amplexus was especially represented in the Neotropical and Mediterranean regions. Most events involved three species-rich globally distributed families (Bufonidae, Ranidae, and Hylidae) but misdirected amplexus was widespread in the phylogeny. We provide a comprehensive data set of misdirected amplexus for anurans, with our results showing that it occurs extensively in the wild and across the globe. This data set provides a baseline for understanding misdirected amplexus and their spatial, temporal, and phylogenetic patterns. Likewise, this data set offers a baseline to test the environmental, ecological, and ethological drivers behind this reproductive behavior and we encourage researchers to report detailed observations of misdirected amplexus to better understand this process and its potential costs at the individual and population levels. The data are not copyright restricted; this data paper should be cited when data are used for publication, and the authors would appreciate being notified of research projects or teaching purposes when these data are used.

Mate-guarding duration is mainly influenced by the risk of sperm competition and not by female quality in a golden orb-weaver spider.

Males are expected to mate with as many females as possible, but can maximize their reproductive success through strategic mating decisions. For instance, males can increase their own fitness by mating with high quality females that produce more offspring. Additionally, males can adjust mating effort based on the relative distribution of females and male competitors. To test factors that influence male mate choice, we assessed male mating decisions in the golden silk orb-weaver spider, Trichonephila clavipes (Nephilidae), a species in which females are polyandrous, males guard females before and after copulation occurs and large males are the most successful at guarding mates. We tested the hypothesis that males spend more time guarding high quality females that are spatially isolated, and when the risk of sperm competition is higher. We also hypothesized that this effect increases with male body size. We assessed solitary and aggregated female webs in the field and quantified female quality (i.e., female body condition), male size (i.e., male body size), the risk of sperm competition (i.e., number of males in each female web), and mate-guarding duration (i.e., number of days each male spent in each web). We found that mate-guarding behaviour is largely influenced by the presence of male competitors. In addition, male body size seems to moderately influence male guarding decisions, with larger males guarding for a longer time. Finally, female body condition and type of web (i.e., solitary or aggregated) seem to play small roles in mate-guarding behaviour. As mate-guarding duration increased by 0.718 day per each additional male competitor in the web, and guarding behaviour prevents males from seeking additional mates, it seems that guarding females can be considerably costly. We conclude that failing to guard a sexual partner promotes high costs derived from sperm competition, and a male cannot recover his relative loss in fertilization success by seeking and fertilizing more females. In addition, the search for more sexual partners can be constrained by possible high costs imposed by weight loss and fights against other males, which may explain why the type of web only moderately influenced male mate choice. Following the same rationale, if high-quality females are not easy to find and/or mating with a high-quality female demands much effort, males may search females and guard them regardless of female quality. In conclusion, the factor that most influences male mate-guarding behaviour among T. clavipes in the field is the risk of sperm competition.

The attraction trick: males in early stages of disease become more chemically attractive to Nile tilapia (Oreochromis niloticus) females.

In aquatic systems, olfaction plays an important role in acquiring information about the social environment and influences important behaviours in various contexts, including predator avoidance, foraging, aggressive and reproductive behaviour and mate selection. As the presence of diseases might modify individual odour, fish may use the variability in conspecifics' odours as an indicator of the health status and infectious load of potential mates. Here, female Nile tilapia were tested for their ability to detect infected males and discriminate between bacterial infected and uninfected individuals by means of chemical cues. Females were allowed to choose between the odours of males infected by Aeromonas hydrophila bacteria and uninfected males. The findings show that female Nile tilapia initially showed a preference for infected males in terms of their first choice in a dichotomous choice test, but the total duration of time spent with the stimulus from infected males was not longer than that for the uninfected males. This may indicate that males at early stages of infection, i.e., without advanced clinical signs of infection, emit odours that allow them to enjoy the benefits of socialization when the infection is not yet detected by conspecifics. Thus, in the context of reproduction, males might attract female partners and have some chance of reproducing, before being avoided.

Differential allocation in a gift-giving spider: males adjust their reproductive investment in response to female condition.

BACKGROUND: When males are selective, they can either reject low-quality females or adjust their reproductive investment in response to traits that indicate female quality (e.g., body size or condition). According to the differential allocation hypothesis, males increase their reproductive investment when paired with high-quality females (positive differential allocation) or increase their reproductive investment when paired with low-quality females (negative differential allocation). This hypothesis has been proposed for monogamous species with biparental care, and most empirical studies focus on birds. Here we used the polygamous spider Paratrechalea ornata, in which males offer prey wrapped in silk as nuptial gifts, to test whether males adjust their reproductive investment in gift size, pre-copulatory and copulatory courtship, and sperm transfer in response to female body condition. RESULTS: Males exposed to females in good body condition added more flies to the gift, stimulated these females longer with abdominal touches during pre-copulatory courtship, and had longer pedipalp insertions than males exposed to females in poor body condition. Female condition affected neither silk investment in nuptial gift wrapping nor the quantity of sperm transferred by males. Finally, females in good body condition oviposited faster after copulation and laid more eggs than females in poor body condition. CONCLUSIONS: We provide experimental evidence that males of a gift-giving spider exhibit positive differential allocation in three key aspects of their reproductive investment: the size of the nutritious gift, duration of pre-copulatory courtship, and duration of pedipalp insertions, which is regarded as a form of copulatory courtship in spiders. This positive differential allocation is likely associated with the benefits of copulating with females in good body condition. These females are more fecund and oviposit faster after copulation than females in poor body condition, which under natural field conditions probably reduces the risk of multiple matings and thus the level of sperm competition faced by the males. As a final remark, our findings indicate that the hypothesis of differential allocation also applies to species with a scramble competition mating system, in which males heavily invest in nuptial gift construction, but not in parental care.

Assortative mating in space and time: patterns and biases.

Despite the important roles of assortative mating for understanding evolutionary processes, our knowledge on the variation in assortative mating across populations and breeding periods has been overshadowed by the greater attention given to general patterns. Obtaining data on mating pairs are difficult for most species; therefore, researchers often group data from different populations or breeding periods, which can increase positive biases in detecting and estimating assortative mating. We used a meta-analytic approach to investigate the biases caused by spatially or temporally pooling data and the assortative mating consistency across populations and breeding periods. We describe assortative mating patterns across and within animal taxa. We performed a systematic review to search studies reporting measures of size-assortative mating (SAM). Grouping data from multiple populations and seasons incurred positive biases. Overall, assortative mating moderately exhibited low repeatability in space and time, but it was inconsistent for most taxa. After excluding pooled measures, the average estimate for assortative mating was moderate and positive. Thus, our findings demonstrate that pooling data can produce misleading results. We also highlight the importance of further investigation of hypotheses that explain spatial and temporal variation in assortative mating, after its detection. Our study reinforces the significance of investigating mating patterns at various spatial and temporal scales before drawing broad conclusions.

Within-population variation in female mating preference affects the opportunity for sexual selection and the evolution of male traits, but things are not as simple as expected.

Females from the same population usually have phenotypic variation in their mating preferences. However, the effects of this within-population variation on the sexual selection acting on males are still unclear. We used individual-based models to explore how within-population variation in female preference (i.e. which male trait value is preferred) and preference strength (i.e. how strong the preference is) affects the opportunity for sexual selection (Is ) and the evolution of a sexually selected male trait. We found the highest Is values when females had high variation in preference and an open-ended preference function. The lowest Is occurred when the magnitude of variation in female preference and male trait value were the same and preference function was closed. Male trait exaggeration was higher when there was high within-population variation in preference and females had an open-ended preference function. Also, higher male trait variation was maintained by high variation in preference, but only for a closed preference function. Thus, we found that only within-population variation in female preference, not in preference strength, influences the opportunity for sexual selection and the evolution of sexually selected male traits. Moreover, we found that the shape of the preference function (i.e. open-ended or closed) and the magnitude of within-population variation in female preference compared to male trait variation also influences the Is and consequently the evolution of male traits.

Chemical signals act as the main reproductive barrier between sister and mimetic Heliconius butterflies.

Colour pattern is the main trait that drives mate recognition between Heliconius species that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related species Heliconius melpomene malleti and H. timareta florencia occur in the same geographical region, and despite being co-mimics, they display strong reproductive isolation. In order to test which cues differ between species, and potentially contribute to reproductive isolation, we quantified differences in the wing phenotype and the male chemical profile. As expected, the wing colour pattern was indistinguishable between the two species, while the chemical profile of the androconial and genital males' extracts showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that chemical blends and not wing colour pattern drive the preference of females for conspecific males. Also, experiments with hybrid males and females suggested an important genetic component for both chemical production and preference. Altogether, these results suggest that chemicals are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.

Preconceptual paternal environmental stimulation alters behavioural phenotypes and adaptive responses intergenerationally in Swiss mice.

Experimental research has recently revealed that paternal environmental conditions can influence the offspring phenotype through epigenetic mechanisms. However, it is unclear whether these effects impact adaptive responses in the offspring. Environmental enrichment (EE) is a well-established paradigm that promotes neural plasticity. We investigated whether EE in male mice could modify behaviours that are highly relevant for determining adaptive fitness, i.e. spatial memory, attractiveness and social dominance, in the offspring of outbred mice. Male Swiss mice were housed in either EE or standard housing from post-weaning to adulthood before breeding for offspring. Their offspring were raised in standard housing until adulthood then assessed for behavioural, physiological and molecular parameters. F0 male mice exposed to EE had lower body weight, higher adrenal, spleen and hippocampal weights, better novelty processing and spatial learning, greater hippocampal BDNF levels, and higher social dominance. Unexpectedly, their male offspring (F1) showed spatial memory impairment, lowered social dominance and were less attractive to receptive females, compared to controls. These ethologically relevant measures suggest a maladaptive response in the male F1 offspring. Interestingly, when separate cohorts of male F1 offspring of standard housing or EE fathers were exposed to 8-day EE protocol during adulthood, differences in spatial memory and attractiveness to receptive females were no longer observed between them. These results provide evidence that the paternal environment can influence the offspring's adaptiveness.

Fear of Violence among Colombian Women Is Associated with Reduced Preferences for High-BMI Men.

Recent studies reveal that violence significantly contributes to explaining individual's facial preferences. Women who feel at higher risk of violence prefer less-masculine male faces. Given the importance of violence, we explore its influence on people's preferences for a different physical trait. Masculinity correlates positively with male strength and weight or body mass index (BMI). In fact, masculinity and BMI tend to load on the same component of trait perception. Therefore we predicted that individuals' perceptions of danger from violence will relate to preferences for facial cues to low-BMI. In two studies in Colombia, men and women from Bogota, Medellin, and surrounding communities were shown pairs of faces transformed to epitomize the shape correlates of men with high or low-BMI. The images were of European, Salvadoran, or Colombian men. Participants were asked to choose the face they considered most attractive. Subsequently, participants answered a survey about their health (e.g., frequency of illnesses the past year), media access (e.g., frequency of Internet use), education level (e.g., graduating from high school), and experiences/perceptions of violence in study 1 and about specific types of violence (public and domestic) in study 2. Results from both studies showed that women who experienced/perceived higher levels of violence preferred faces of low-BMI Salvadoran men. Preferences for low-BMI facial cues were significantly explained by violence (public or domestic), even after controlling for all other variables (including age, education, health, and media access). These results may reflect women's strategy to avoid male partners capable of inflicting harm.

Chemosensory discrimination of male age by female Psammodromus algirus lizards based on femoral secretions and feces

Chemical communication plays an essential role in several social and reproductive behaviors of many animals. In lizards, the main sources of semiochemicals are femoral or pre-anal gland secretions and feces. In male lizards Psammodromus algirus, there are age-related differences in the chemical composition of femoral gland secretions and in the reproductive strategies, with older males defending territories and females, while younger males adopting sneak-mating strategies. Females flee more often from mating advances of young males than from those of old males, which are more successful in obtaining matings. This suggests that age discrimination of males may be important for females. We tested here whether females showed differential chemosensory responses to chemical cues (femoral gland secretion and feces) of males of two age classes, and whether females use information from substrate scent marks of males of different ages to select where to stay. We found that females elicited more tongue-flicks to the secretion and feces of old males than to control or secretion and feces of young males. Also, the time spent by females on a scented paper depended on the treatment, suggesting that females tended to spend more time on scent marks made with femoral secretions of old males. Adult females seemed capable to discriminate between young and old males based on chemical cues alone and showed more interest in scents of old males. However, substrate scent marks did not seem to entirely determine site selection by females, suggesting that females might need additional cues to perform the choice. These results can be explained by the different age-dependent reproductive strategies of males, which can affect differentially to females.

Test of the Deception Hypothesis in Atlantic Mollies Poecilia mexicana-Does the Audience Copy a Pretended Mate Choice of Others?

Animals often use public information for mate-choice decisions by observing conspecifics as they choose their mates and then copying this witnessed decision. When the copier, however, is detected by the choosing individual, the latter often alters its behavior and spends more time with the previously non-preferred mate. This behavioral change is called the audience effect. The deception hypothesis states that the choosing individual changes its behavior to distract the audience from the preferred mate. The deception hypothesis, however, only applies if the audience indeed copies the pretended mate choice of the observed individual. So far, this necessary prerequisite has never been tested. We investigated in Atlantic molly males and females whether, first, focal fish show an audience effect, i.e., alter their mate choices in the presence of an audience fish, and second, whether audience fish copy the mate choice of the focal fish they had just witnessed. We found evidence that male and female Atlantic mollies copy the pretended mate choice of same-sex focal fish. Therefore, a necessary requirement of the deception hypothesis is fulfilled. Our results show that public information use in the context of mate choice can be costly.

The influence of developmental environment on courtship song in cactophilic Drosophila.

Closely related species often differ in the signals involved in sexual communication and mate recognition. Determining the factors influencing signal quality (i.e. signal's content and conspicuousness) provides an important insight into the potential pathways by which these interspecific differences evolve. Host specificity could bias the direction of the evolution of sexual communication and the mate recognition system, favouring sensory channels that work best in the different host conditions. In this study, we focus on the cactophilic sibling species Drosophila buzzatii and D. koepferae that have diverged not only in the sensory channel used for sexual communication and mate recognition but also in the cactus species that use as primary hosts. We evaluate the role of the developmental environment in generating courtship song variation using an isofemale line design. Our results show that host environment during development induces changes in the courtship song of D. koepferae males, but not in D. buzzatii males. Moreover, we report for the first time that host rearing environment affects the conspicuousness of courtship song (i.e. song volume). Our results are mainly discussed in the context of the sensory drive hypothesis.

Mating system, age, and reproductive performance in Tenuisvalvae notata, a long-lived ladybird beetle.

The long-lived polygynandrous ladybird beetle Tenuisvalvae notata (Mulsant) found in Brazil was evaluated in the laboratory for the effects of multiple mating and aging on its reproductive performance. This species is native to South America and is an important predator of mealybugs. Specifically studied were partner choice, female reproductive success, adult longevity, male virility, and offspring development. Young (5-10 days old) and older virgin females (95-100 days old) were subjected to either a single mate or multiple mating with the same or different males of various mating status (virgin or previously mated once, twice, and thrice). Results revealed a preference in both genders to mate with previously known partners. Additionally, younger females had higher fecundity and greater longevity when mated only once in comparison to those mated multiple times. Fecundity, fertility, and offspring development were similar across the treatments regardless of the number of mating or male mating history. Fecundity and fertility decreased throughout the oviposition period regardless of mating treatment.

Female Brazilian whiptail lizards (Cnemidophorus ocellifer) prefer males with high ultraviolet ornament reflectance.

Conspicuous colouration is an important way of social communication in many taxa. The role of ultraviolet (UV) signals in intraspecific communication has only recently been studied in lizards, and there is not a general understanding of the adaptive role of UV colouration. Colour ornaments can signal male quality in mate choice and are therefore suitable for reliably predicting the outcome of female preference. Here, we tested the potential role of UV colouration in female spatial preference in a non-territorial teiid lizard, Cnemidophorus ocellifer. We experimentally manipulated the UV reflectance of size-matched male pairs and tested the effects of our treatment on females' spatial distribution. We found that females associated with males of higher UV reflectance, suggesting that UV colour can be an important clue during mate preference decisions. Our results provide the first empirical evidence for the importance of UV colouration in female preference in a mutually ornamented lizard species.

Testosterone, the progesterone/estradiol ratio, and female ratings of masculine facial fluctuating asymmetry for a long-term relationship.

Idiosyncratic variation within the normal range of androgens levels in women account for significant variations in personality and behavior. We studied if testosterone introduces significant biases in women's perception of fluctuating symmetry of male faces suitability for a long-term relationship. Participants were 145 female college students asked to rate in a two-choice forced paradigm the attractiveness, suitability as a long-term partner, and economic success, fatherliness and fidelity of an asymmetric and a symmetric male face. Since our sample consists of random women interested in participating, whether for personal reasons or because they were paid to participate, we controlled for menstrual phase. All participants provided salivary samples to determine testosterone (T), estradiol (E2) and progesterone (P4) levels. When the P4/E2 was low and T low-to-normal, the symmetric face was rated as more attractive, and a desirable long-term partner, but these preferences changed to the opposite when P4/E2 was high. In high T women, neither face was rated as more attractive, independently from the P4/E2 ratio, but the asymmetric face was preferred as a long-term partner when conception risk was high, changing to prefer the symmetric face as the P4/E2 increased. The overall perception of male faces was that the symmetric face was more economical successful but a poor parent and highly unfaithful compared to the asymmetric face. A significant interaction between T and P4/E2 for ratings success of the asymmetric face suggests that high levels of feminine T might be related to inter-sexual competition when conception risk is high.

Genetic population structure in an equatorial sparrow: roles for culture and geography.

Female preference for local cultural traits has been proposed as a barrier to breeding among animal populations. As such, several studies have found correlations between male bird song dialects and population genetics over relatively large distances. To investigate whether female choice for local dialects could act as a barrier to breeding between nearby and contiguous populations, we tested whether variation in male song dialects explains genetic structure among eight populations of rufous-collared sparrows (Zonotrichia capensis) in Ecuador. Our study sites lay along a transect, and adjacent study sites were separated by approximately 25 km, an order of magnitude less than previously examined for this and most other species. This transect crossed an Andean ridge and through the Quijos River Valley, both of which may be barriers to gene flow. Using a variance partitioning approach, we show that song dialect is important in explaining population genetics, independent of the geographic variables: distance, the river valley and the Andean Ridge. This result is consistent with the hypothesis that song acts as a barrier to breeding among populations in close proximity. In addition, songs of contiguous populations differed by the same degree or more than between two populations previously shown to exhibit female preference for local dialect, suggesting that birds from these populations would also breed preferentially with locals. As expected, all geographic variables (distance, the river valley and the Andean Ridge) also predicted population genetic structure. Our results have important implications for the understanding whether, and at what spatial scale, culture can affect population divergence.