Mating Environments Research Articles

Mating environments mediate the evolution of behavioral isolation during ecological speciation.

The evolution of behavioral isolation is often the first step toward speciation. While past studies show that behavioral isolation will sometimes evolve as a by-product of divergent ecological selection, we lack a more nuanced understanding of factors that may promote or hamper its evolution. The environment in which mating occurs may be important in mediating whether behavioral isolation evolves for two reasons. Ecological speciation could occur as a direct outcome of different sexual interactions being favored in different mating environments. Alternatively, mating environments may vary in the constraint they impose on traits underlying mating interactions, such that populations evolving in a "constraining" mating environment would be less likely to evolve behavioral isolation than populations evolving in a less constraining mating environment. In the latter, mating environment is not the direct cause of behavioral isolation but rather permits its evolution only if other drivers are present. We test these ideas with a set of 28 experimental fly populations, each of which evolved under one of two mating environments and one of two larval environments. Counter to the prediction of ecological speciation by mating environment, behavioral isolation was not maximal between populations evolved in different mating environments. Nonetheless, mating environment was an important factor as behavioral isolation evolved among populations from one mating environment but not among populations from the other. Though one mating environment was conducive to the evolution of behavioral isolation, it was not sufficient: assortative mating only evolved between populations adapting to different-larval environments within that mating environment, indicating a role for ecological speciation. Intriguingly, the mating environment that promoted behavioral isolation is characterized by less sexual conflict compared to the other mating environment. Our results suggest that mating environments play a key role in mediating ecological speciation via other axes of divergent selection.

The evolution of sexual dimorphism in gene expression in response to a manipulation of mate competition.

Many genes are differentially expressed between males and females and patterns of sex-biased gene expression (SBGE) vary among species. Some of this variation is thought to have evolved in response to differences in mate competition among species that cause varying patterns of sex-specific selection. We used experimental evolution to test this by quantifying SBGE and sex-specific splicing in 15 Drosophila melanogaster populations that evolved for 104 generations in mating treatments that removed mate competition via enforced monogamy, or allowed mate competition in either small, simple, or larger, structurally more complex mating environments. Consistent with sex-specific selection affecting SBGE, initially sex-biased genes diverged in expression more among treatments than unbiased genes, and there was greater expression divergence for male- than female-biased genes. It has been suggested the transcriptome should be "feminized" under monogamy because of the removal of sexual selection on males; we did not observe this, likely because selection differs in additional ways between monogamy vs. polygamy. Significant divergence in average expression dimorphism between treatments was observed and, in some treatment comparisons, the direction of the divergence differed across different sex-bias categories. There was not a generalized reduction in expression dimorphism under enforced monogamy.

Male reproductive success is not strongly affected by phenological changes in mate availability in monoecious Sagittaria latifolia.

Many plants express their female and male sex roles at different times (dichogamy), with important consequences for mating. Dichogamy can yield mate limitation via biased floral sex ratios, particularly at the beginning and end of the flowering season when many plants simultaneously function as the same sex. This form of mate limitation should be reduced if plants adjust their allocations to female versus male sex functions in a manner that tracks seasonal variability in mating opportunities. For example, under protogyny (i.e. dichogamy with female function expressed first) plants with male-biased sex expression should have enhanced mating opportunities early in the flowering season as other plants begin to flower (in female sex phase). We quantified seasonal changes in sex allocation, patterns of mate availability and realized siring success in a population of protogynous Sagittaria latifolia. Our results were consistent with previous findings that seasonal changes in sex allocation should compensate for lost mating opportunities under the temporally variable mating environments caused by dichogamy. However, patterns of siring success in the population were inconsistent with this interpretation. We suggest that realized siring success might depend more strongly on spatial than on temporal aspects of mate availability.

An investigation of the sex-specific genetic architecture of fitness in Drosophila melanogaster.

In dioecious populations, the sexes employ divergent reproductive strategies to maximize fitness and, as a result, genetic variants can affect fitness differently in males and females. Moreover, recent studies have highlighted an important role of the mating environment in shaping the strength and direction of sex-specific selection. Here, we measure adult fitness for each sex of 357 lines from the Drosophila Synthetic Population Resource in two different mating environments. We analyze the data using three different approaches to gain insight into the sex-specific genetic architecture for fitness: classical quantitative genetics, genomic associations, and a mutational burden approach. The quantitative genetics analysis finds that on average segregating genetic variation in this population has concordant fitness effects both across the sexes and across mating environments. We do not find specific genomic regions with strong associations with either sexually antagonistic (SA) or sexually concordant (SC) fitness effects, yet there is modest evidence of an excess of genomic regions with weak associations, with both SA and SC fitness effects. Our examination of mutational burden indicates stronger selection against indels and loss-of-function variants in females than in males.

Sperm allocation in relation to male–male aggression and courtship in an externally fertilizing fish, the medaka

Sperm production is physiologically costly; therefore, males that mate multiple times are expected to allocate sperm prudently to maximize their fitness. Sperm allocation theory has been widely tested in internally fertilizing animals; however, few studies have investigated whether males adjust the number of sperm released according to their premating experience and cues from rival males. Here, we investigated sperm allocation strategies in an externally fertilizing fish, the medaka, Oryzias latipes, in controlled conditions. We used three treatments: direct interaction with a rival (two males were allowed to interact directly with each other), visual cue only (presenting a male in a separate compartment) and no rivals (control). In the direct interaction treatment, two types of alternative male mating behaviour, simultaneous sperm release and postspawn sperm release, were observed. Premating experiences affected subsequent mating behaviour: males that were more aggressive and exhibited more prominent courtship behaviour mated females without any disturbance from the other males, whereas simultaneous sperm release frequently occurred when both males exhibited similar levels of aggression and courtship behaviours. We also counted the sperm released per mating from the water tank. There was no change in the number of sperm released in the presence of visual cues of competition or direct interaction with the other males before mating. However, males (focal and/or rival) released more sperm only when sperm competition was high, that is, when a rival male successfully disrupted mating before simultaneous sperm release. Our results indicate that medaka males may adjust the number of sperm released per mating in different mating environments.

Complex vocal learning and three-dimensional mating environments

Complex vocal learning, the capacity to imitate new sounds, underpins the evolution of animal vocal cultures and song dialects and is a key prerequisite for human speech and song. Due to its relevance for the understanding of cultural evolution and the biology and evolution of language and music, the trait has gained much scholarly attention. However, while we have seen tremendous progress with respect to our understanding of its morphological, neurological and genetic aspects, its peculiar phylogenetic distribution has remained elusive. Intriguingly, animals as distinct as hummingbirds and humpback whales share well-developed vocal learning capacity in common with humans, while this ability is quite limited in nonhuman primates. Yet, solving this ‘vocal learning conundrum’ may shed light on the constraints ancestral humans overcame to unleash their vocal capacities. To this end I consider major constraints and functions that have been proposed. I highlight an especially promising ecological constraint, namely the spatial dimensionality of the environment. Based on an informal comparative review, I suggest that complex vocal learning is associated with three-dimensional habitats such as air and water. I argue that this is consistent with recent theoretical advances—i.e., the coercion-avoidance and dimensionality hypotheses—and with the long-standing hypothesis that mate choice is a major driver of the evolution and origin of complex vocal learning. However, I stress that multiple functions may apply and that quantitative phylogenetic comparative methods should be employed to finally resolve the issue.

Predator‐induced maternal and paternal effects independently alter sexual selection

Parental experience alters survival-related phenotypes of offspring in both adaptive and nonadaptive ways, yielding rapid inter- and transgenerational fitness effects. Yet, fitness comprises survival and reproduction, and parental effects on mating decisions could alter the strength and direction of sexual selection, affecting long-term evolutionary trajectories. We used a full factorial design in which threespine stickleback (Gasterosteus aculeatus) mothers, fathers, both, or neither were exposed to a model predator at developmentally appropriate times to test for predator-induced maternal, paternal, and joint parental effects on daughters' mating behavior. We tested the responsiveness, preferences, and mate choices of adult daughters in no-choice trials with wild-caught males who had varied sexual signals. Maternal and paternal predator exposure independently yielded daughters who preferred males who were intermediate in conspicuousness (with duller nuptial coloration and who courted less vigorously), relaxing the typical preference for the most conspicuous males. The combined effects of maternal and paternal predator exposure were not cumulative; when both parents were predator exposed, single-parent effects on mate preferences were reversed. Thus, we cannot assume that maternal and paternal effects additively combine to produce "parental" effects. Further, joint parental predator exposure yielded daughters who were three times less likely to mate at all. Stress-induced intergenerational parental effects on reproductive decisions such as those observed here may potentiate rapid transgenerational responses to novel and changing mating environments.

Testing for local adaptation in adult male and female fitness among populations evolved under different mate competition regimes.

Mating/fertilization success and fecundity are influenced by sexual interactions among individuals, the nature and frequency of which can vary among different environments. The extent of local adaptation for such adult fitness components is poorly understood. We allowed 63 populations of Drosophila melanogaster to independently evolve in one of three mating environments that alter sexual interactions: one involved enforced monogamy, while the other two permitted polygamy in either structurally simple standard fly vials or in larger "cages" with added complexity. Adult male and female reproductive fitness were measured after 16 and 28 generations, respectively, via full reciprocal transplants. In males, reciprocal local adaptation was observed between the monogamy and simple polygamy treatments, consistent with the evolution of reproductively competitive males under polygamy that perform poorly under monogamy because they harm their only mate. However, males evolved in the complex polygamy treatment performed similarly or better than all other males in all mating environments, consistent with previous results showing higher genetic quality in this treatment. Differences in female fitness were more muted, suggesting selection on females was less divergent across the mating treatments and echoing a common pattern of greater phenotypic and expression divergence in males than females.

Sequential decline in fruit resource allocation within inflorescences of Sagittaria trifolia: a test of non‐uniform pollination hypothesis

AbstractFlowering plants often exhibit declining resource investment to floral organs, fruits and seeds temporally or spatially in an inflorescence. To account for such variances, non‐uniform pollination hypothesis, which highlights various mating environments each flower experiences, provides adaptive significance for allocation patterns but with controversial supports. Sagittaria trifolia (Alismataceae) was used to examine differences in seed number, seed weight and germination rate among sequential fruits within inflorescences. Ovule number was also investigated to evaluate allocation patterns in the floral stage. To test the non‐uniform pollination hypothesis, we used three polymorphic microsatellite loci of S. trifolia to estimate the seed outcrossing rate in proximal and distal fruits. The results showed that the seed number, average seed weight and seed germination rate of S. trifolia gradually decreased from proximal to distal fruits within inflorescences. The percent of decrease in seed number between two contiguous fruits was 14.68 ± 3.22%, which was much stronger than the percent of decrease in ovule number at 6.95 ± 1.60%. Both proximal and distal fruits within inflorescences had high outcrossing rates (81.5 ± 5.0%, proximal; 82.3 ± 6.9%, distal) and they did not differ significantly. Overall, there was an acropetal decline of resource allocation to fruits within inflorescences of S. trifolia. Allocation pattern to ovules was not a limiting factor for seed production. The lack of difference in outcrossing rate between proximal and distal fruits indicated that the allocation strategy was probably not caused by non‐uniform pollination, but more likely position effects.

Acute effects of sex steroids on visual processing in male goldfish.

Elevations of sex steroids induced by social cues can rapidly modulate social behavior, but we know little about where they act within the nervous system to produce such effects. In male goldfish, testosterone (T) rapidly increases approach responses to the visual cues of females through its conversion to estradiol. Because aromatase is expressed in the retina, we tested if T can acutely influence retina responses to visual stimuli, and investigated the receptor mechanisms that may mediate such effects. Specifically, we measured FOS protein immunoreactivity to determine if T affects cellular responses to visual stimuli that include females, and used electrophysiology to investigate whether T can generally affect light sensitivity. We found that T acutely increased FOS responses to the simultaneous onset of light and the presence of female visual stimuli, both of which would normally be associated with early morning spawning, and increased electrophysiological responses to low intensity light pulses. Both effects were blocked by an estrogen receptor beta (ERβ) antagonist, indicating that T is likely being converted to estradiol (E2) and acting through an ERβ mediated mechanism to acutely modulate visual processing. Changes in sensory processing could subsequently influence approach behavior to increase reproductive success in competitive mating environments.

The purging of deleterious mutations in simple and complex mating environments

There is a general expectation that sexual selection should align with natural selection to aid the purging of deleterious mutations, yet experiments comparing purging under monogamy versus polygamy have provided mixed results. Recent studies suggest that this may be because the simplified mating environments used in these studies reduce the benefit of sexual selection through males and hamper natural selection through females by increasing costs associated with sexual conflict. To test the effect of the physical mating environment on purging, we use experimental evolution in Drosophila melanogaster to track the frequency of four separate deleterious mutations in replicate populations that experience polygamy under either a simple or structurally complex mating arena while controlling for arena size. Consistent with past results suggesting a greater net benefit of polygamy in a complex environment, two of the mutations were purged significantly faster in this environment. The other two mutations showed no significant difference between environments.

Environmental complexity and the purging of deleterious alleles.

Sexual interactions among adults can generate selection on both males and females with genome-wide consequences. Sexual selection through males is one component of this selection that has been argued to play an important role in purging deleterious alleles. A common technique to assess the influence of sexual selection is by a comparison of experimental evolution under enforced monogamy versus polygamy. Mixed results from past studies may be due to the use of highly simplified laboratory conditions that alter the nature of sexual interactions. Here, we examine the rate of purging of 22 gene disruption mutations in experimental polygamous populations of Drosophila melanogaster in each of two mating environments: a simple, high-density environment (i.e., typical fly vials), and a lower density, more spatially complex environment. Based on past work, we expect sexual interactions in the latter environment to result in stronger selection in both sexes. Consistent with this, we find that mutations tend to be purged more quickly in populations evolving in complex environments. We discuss possible mechanisms by which environmental complexity might modulate the rate at which deleterious alleles are purged and putatively ascribe a role for sexual interactions in explaining the treatment differences in our experiment.

How the Dark Triad traits predict relationship choices

While previous studies have correlated the Dark Triad traits (i.e., narcissism, psychopathy, and Machiavellianism) with a preference for short-term relationships, little research has addressed possible correlations with short-term relationship sub-types. In this online study using Amazon’s Mechanical Turk system (N=210) we investigated the manner in which scores on the Dark Triad relate to the selection of different mating environments using a budget-allocation task. Overall, the Dark Triad were positively correlated with preferences for short-term relationships and negatively correlated with preferences for a long-term relationship. Specifically, narcissism was uniquely correlated with preferences for one-night stands and friends-with-benefits and psychopathy was uniquely correlated with preferences for booty-call relationships. Both narcissism and psychopathy were negatively correlated with preferences for serious romantic relationships. In mediation analyses, psychopathy partially mediated the sex difference in preferences for booty-call relationships and narcissism partially mediated the sex difference in preferences for one-night stands. In addition, the sex difference in preference for serious romantic relationships was partially mediated by both narcissism and psychopathy. It appears the Dark Triad traits facilitate the adoption of specific mating environments providing fit with people’s personality traits.

Enigmatic ornamentation eases male reliance on courtship performance for mating success

Female preferences are frequently invoked to explain the widespread occurrence of elaborate male ornaments, yet empirical data demonstrating such preferences are sometimes equivocal or even contradictory. In the wolf spider Schizocosa stridulans, despite evidence of strong female choice, prior research has been unable to link the conspicuous sexually dimorphic foreleg ornamentation of males to their mating success. We conducted three experiments aimed at determining the function of this previously enigmatic ornamentation. Our first two experiments used males with phenotypically modified foreleg phenotypes in simple and complex mating environments in order to examine the relationship between the presence/absence of ornamentation and male mating success. In both experiments, we found no relationship: courtship rate was the sole predictor of mating success. In a third experiment, we used males with naturally varying foreleg ornamentation in mating trials. Ornamentation was subsequently quantified and we again examined the factors influencing male mating success. As in our first two experiments, we found courtship rate to be a good predictor of mating success. Additionally, we discovered that foreleg ornamentation and courtship rate interact to influence male mating success. At low courtship rates, males with more foreleg ornamentation have a mating advantage, whereas at high courtship rates, males with less foreleg ornamentation have a mating advantage. We discuss several potential explanations for these results. In summary, we provide the first evidence of a benefit of foreleg ornamentation in male S. stridulans and suggest that this benefit is realized by the interaction between ornamentation and courtship rate.

THE ROLE OF MULTILEVEL SELECTION IN THE EVOLUTION OF SEXUAL CONFLICT IN THE WATER STRIDER AQUARIUS REMIGIS

In evolution, exploitative strategies often create a paradox in which the most successful individual strategy "within" the group is also the most detrimental strategy "for" the group, potentially resulting in extinction. With regard to sexual conflict, the overexploitation of females by harmful males can yield similar consequences. Despite these evolutionary implications, little research has addressed why sexual conflict does not ultimately drive populations to extinction. One possibility is that groups experiencing less sexual conflict are more productive than groups with greater conflict. However, most studies of sexual conflict are conducted in a single isolated group, disregarding the potential for selection among groups. We observed Aquarius remigis water striders in a naturalistic multigroup pool in which individuals could freely disperse among groups. The free movement of individuals generated variation in aggression and sex-ratio among groups, thereby increasing the importance of between-group selection compared to within-group selection. Females dispersed away from local aggression, creating more favorable mating environments for less-aggressive males. Furthermore, the use of contextual analysis revealed that individual male aggression positively predicted fitness whereas aggression at the group level negatively predicted fitness, empirically demonstrating the conflict between levels of selection acting on mating aggression.

Sexual Strategies Across Sexual Orientations

Abstract The psychological intersection of biological sex, personality, and sexual orientation represents a unique prospect for investigating the evolution of human mating strategies. Evolved sex differences in human psychology may encounter different mating environments within homosexual and heterosexual contexts. The personality traits of homosexuals, if different from heterosexuals, may influence human mating dynamics in revealing ways. In the current study, 5,310 men (5,083 heterosexuals, 131 homosexuals, and 96 bisexuals) and 7,589 women (7,240 heterosexuals, 143 homosexuals, and 206 bisexuals) across four major world regions completed personality and sexuality self-report surveys. Consistent with previous research, sociosexual behavior (e.g., number of one-night stands) and personality traits (e.g., masculinity and openness to experience) varied across sexual orientation. In addition, personality traits were predictably related to sociosexual behavior. However, variability in personality traits did ...

THE ROLES OF NATURAL AND SEXUAL SELECTION DURING ADAPTATION TO A NOVEL ENVIRONMENT

The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.

Quantitative analysis of group II intron expression and splicing in Lactococcus lactis.

The group II intron Ll.ltrB is found within the ltrB relaxase gene of the conjugative element pRS01 in Lactococcus lactis. Precise splicing of the intron is essential for pRS01 transfer. The transcription regulation and in vivo splicing activity of Ll.ltrB have not been investigated thoroughly in L. lactis in the natural pRS01 context. We developed absolute quantitative real-time reverse transcription-PCR assays to quantify RNA levels of the 5' exon (ltrBE1) and the spliced relaxase (ltrB) and intron-encoded protein (ltrA) genes, as well as Ll.ltrB splicing activity under different physiological conditions. The mRNA levels for the ATP-binding protein OppD were assayed for comparison to the ltrB transcripts. The oppD mRNA ranged from 10- to 10,000-fold higher than ltrB region genes. ltrBE1 expression was growth-phase dependent. The mRNA level of ltrA was almost constant during all growth phases and in all media tested. Ll.ltrB in vivo splicing activity ranged from (6.5 +/- 2.1)% to (22.1 +/- 8.0)%. Acid challenge significantly decreased both ltrB region mRNA levels and intron splicing activity. The presence of recipient cells, different mating environments, and temperature stress had no significant effects on expression and splicing. Western blotting showed that the level of LtrB protein expressed from an intronless ltrB gene was much higher (about 20-fold) than the level of protein expressed from an intron-containing construct. Interestingly, LtrB protein showed a tendency to function in cis on its oriT target. The low level of ltrB transcript and relatively inefficient splicing of the intron may limit Ll.ltrB mobility and dissemination in nature.

Environmental Predictors of Geographic Variation in Human Mating Preferences

Sexual selection theory classically posits consistent and directional mate‐preferences for male traits that provide benefits to females. However, flexible mate‐choice tactics may persist within a species when males display multiple desirable features that confer different benefits to females under variable environmental conditions. Ecological factors such as population density, resource demand, and sex ratio can influence the value that female animals place on certain male characteristics across mating environments. In this study, I used human mate‐preference data from `lonely hearts' advertisements in the newspapers of 23 cities in the USA to assess geographic differences in female preferences for male traits (e.g. physical attributes, resource‐holding potential, emotional characteristics, personal interests) in relation to these ecological parameters. I found that females placed more emphasis on the resource‐accruing ability of prospective mates in densely populated cities and cities having greater resource demands (higher cost of living). In contrast, women from densely populated or resource‐demanding cities placed less emphasis on the emotional aspects or personal interests of males. Preferences for physical features were not environmentally linked, but instead were a function of the degree to which females advertised their own physical attractiveness. Collectively, these results suggest that certain mate‐choice criteria employed by women are sensitive to variation in local environmental conditions and that variable levels of resource or mate availability may favor different mating tactics across human populations.

FLORAL SEX ALLOCATION IN SEQUENTIALLY BLOOMING PLANTS.

In plants whose flowers develop in a sequence, different flowers may exhibit temporal variation in pollen donation and receipt such that the fitness contributions through male and female functions can vary among flowers. Dichogamy, or directional pollinator movements within inflorescences, can create situations where flowers in different stages in the sequence may differ in the numbers of flowers in the female stage available as potential mates. We present an evolutionarily stable strategy (ESS) analysis of the resource allocations expected in different flowers in hermaphroditic plants when the mating environments vary among flowers. This introduces a modular element into sex-allocation models. Our analysis shows that such variation in the mating environments of flowers can select for differences in sex allocation between flowers. When male and female fertilities are nonlinear functions of the allocations, variation in resource availability can also select for variation in sex allocation among flowers. The influence of dichogamy and pollinator directionality on floral sex allocation is discussed, and the empirical evidence supporting the predictions derived from the model is briefly reviewed. The implications of our results for the evolution of andromonoecy and monoecy are discussed.