Female stickleback prefer shallow males: Sexual selection on nest microhabitat

Sexual selection is most often thought of as acting on organismal traits, such as size or color. However, individuals’ habitat use may also affect mating success. Here, we show that, in threespine stickleback, nest depth can be a target of sexual selection. In postglacial lakes in British Columbia, male threespine stickleback nest in a narrow range of depths. Prior studies revealed heritable variation in males’ preferred nest microhabitat. We surveyed four natural populations, finding that male stickleback with shallower nests were more successful at breeding. Indeed, nest depth was a much stronger predictor of male mating success than more commonly studied targets of sexual selection in stickleback (size, condition, shape, color, infection status). This selection on nest depth means that variance in fitness changed predictably across microhabitats, altering the opportunity for sexual selection to act on other traits. Accordingly, we show that sexual selection on other male traits is strongest where variance in nesting success is highest (at intermediate nest depths in some lakes). We conclude that males’ choice of nesting microhabitat is an especially important target of sexual selection, resulting in fine‐scale spatial variation in sexual selection on other traits.     

Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

Correlates of male mating success in the lekking great snipe (Gallinago media): results from a four-year study

To investigate behavioral or morphological traits importantas mate choice cues, we measured selection differentials (s)as the covariances between each trait and male mating success,and directional selection gradients (J3) from multiple linearregression of the standardized traits on male mating success.Data from two leks in four consecutive years were included,and the annual data were analyzed separately. The main findingsare: (1) the distribution of male mating success proved to beless skewed than those found in many other lekking species,(2) only a few traits yielded significant selection gradients,(3) the importance of age on male mating success changed acrossyears, (4) females may use traits with a high variance as matechoice cues, and (5) individual males achieved similar matingsuccesses between years. Attendance and age were the traitsmost consistently correlated with male mating success, but notraits showed significant selection gradients in all years.Our results indicate that variable sexual selection pressuresexisted between years, but the high correlation found betweenthe mating success of individual males in successive seasonsalso indicates that permanent differences in male traits areimportant. Key words: lek, mate choice, sexual selection.     

Sexual selection for male dominance reduces opportunities for female mate choice in the European bitterling (Rhodeus sericeus)

Sexual selection involves two main mechanisms: intrasexual competition for mates and intersexual mate choice. We experimentally separated intrasexual (male-male interference competition) and intersexual (female choice) components of sexual selection in a freshwater fish, the European bitterling (Rhodeus sericeus). We compared the roles of multiple morphological and behavioural traits in male success in both components of sexual competition, and their relation to male reproductive success, measured as paternity of offspring. Body size was important for both female choice and male-male competition, though females also preferred males that courted more vigorously. However, dominant males often monopolized females regardless of female preference. Subordinate males were not excluded from reproduction and sired some offspring, possibly through sneaked ejaculations. Male dominance and a greater intensity of carotenoid-based red colouration in their iris were the best predictors of male reproductive success. The extent of red iris colouration and parasite load did not have significant effects on female choice, male dominance or male reproductive success. No effect of parasite load on the expression of red eye colouration was detected, though this may have been due to low parasite prevalence in males overall. In conclusion, we showed that even though larger body size was favoured in both intersexual and intrasexual selection, male-male interference competition reduced opportunities for female choice. Females, despite being choosy, had limited control over the paternity of their offspring. Our study highlights the need for reliable measures of male reproductive success in studies of sexual selection.     

Is egg carrying attractive? Mate choice in the golden egg bug (Coreidae,Heteroptera)

In several species of fish, females select males that are already guarding eggs in their nests. It is a matter of debate as to whether a female selects a good nest site for her offspring (natural selection) or a male for his attractiveness (sexual selection). The golden egg bug, Phyllomorpha laciniata Vill, resembles fish in the sense that mating males carry more eggs than single males, but in the bugs, female mate choice is decoupled from egg site choice. The sexual selection hypothesis predicts that if females select males using male egg load as a cue for male quality, they should not mate with a male when eggs are removed, regardless of his mating attempts. When individual females were enclosed with an egg-loaded male and an unloaded male, they mated equally often with both males, although the loaded males courted more. In addition, when only successful males were used, females mated equally often with the loaded male and the unloaded male irrespective of sex ratio. Male choice rather than female choice affected mating frequency when sex ratio was equal. Therefore, females do not select the male by the eggs he carries, but successful males may receive many eggs due to egg dumping by alien females while they mate or as a consequence of mate guarding.     

A STATISTICAL STUDY OF MATE CHOICE: SEXUAL SELECTION IN A PLETHODONTID SALAMANDER (DESMOGNATHUS OCHROPHAEUS)

Our experiment revealed the existence of significant variation in mating success in a salamander species in which males do not provide courtship feeding, nest sites, or parental care. Differences in mating success were based on natural variation among adult males and females, rather than on traits of an artificially selected set of potential mates. Courtship encounters deliberately involved only one male and one female, thus eliminating the potentially confounding effects of male-male competition and variations in mate encounter rate. Even after eliminating these effects and random error, some females were more likely than others to elicit spermatophore deposition by a male, and some males were more likely than others to inseminate a female. Such variation among individuals represents an opportunity for sexual selection to act on phenotypic characters that affect mating success. We advocate the use of a factorial experimental design to analyze sexual selection. This approach permits the statistical evaluation of separate male and female effects, interaction between these effects, and random effects. Designs which combine the evaluations of mating success and courtship behaviors could estimate the force of sexual selection on behavior.     

Parasites and Sexual Selection in Birds of Paradise

We studied blood parasite infections in relation to aspectsof sexual selection and mate choice in 10 species of birds ofparadise. Across species there was a significant, positive correlationbetween relative parasite intensity and showiness in males.Parasite infections also correlated across species with thedegree of sexual dimorphism and varied with mating systems.Promiscuous species were showier and had significantly higherparasite prevalences than monogamous species. Within one species,Lawes' Parotia (Parotia lawesii), parasite intensity was negativelycorrelated with all phenotypic traits examined, a pattern significantlydifferent than random. The mating success of males with lowparasite intensities varied, but males with high intensitiesdid not mate. Sampling of individual males on repeated occasionsrevealed large temporal differences in parasite counts whichspanned the range believed to affect behavior and mating success.Whereas the interspecific correlations support one predictionof the Hamilton and Zuk hypothesis on parasites and sexual selection,the intraspecific data are equivocal with respect to a secondprediction of this hypothesis. Parasites appear to influencethe behavior of Lawes' Parotia, but alternative explanationsto that of Hamilton and Zuk for this effect are equally plausibleand there is no evidence of a link between female choice andthe traits in males indicative of parasite loads. We suggestthat female Lawes' Parotia may be avoiding highly infected malesrather than actively choosing parasite-resistant males.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.     

The complex interplay between macronutrient intake,cuticular hydrocarbon expression and mating success in male decorated crickets

The condition dependence of male sexual traits plays a central role in sexual selection theory. Relatively little, however, is known about the condition dependence of chemical signals used in mate choice and their subsequent effects on male mating success. Furthermore, few studies have isolated the specific nutrients responsible for condition‐dependent variation in male sexual traits. Here, we used nutritional geometry to determine the effect of protein (P) and carbohydrate (C) intake on male cuticular hydrocarbon (CHC) expression and mating success in male decorated crickets (Gryllodes sigillatus). We show that both traits are maximized at a moderate‐to‐high intake of nutrients in a P:C ratio of 1 : 1.5. We also show that female precopulatory mate choice exerts a complex pattern of linear and quadratic sexual selection on this condition‐dependent variation in male CHC expression. Structural equation modelling revealed that although the effect of nutrient intake on mating success is mediated through condition‐dependent CHC expression, it is not exclusively so, suggesting that other traits must also play an important role. Collectively, our results suggest that the complex interplay between nutrient intake, CHC expression and mating success plays an important role in the operation of sexual selection in G. sigillatus.     

Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish

Theory suggests that genetic polymorphisms in female mating preferences may cause disruptive selection on male traits, facilitating phenotypic differentiation despite gene flow, as in reinforcement or other models of speciation with gene flow. Very little experimental data have been published to test the assumptions regarding the genetics of mate choice that such theory relies on. We generated a population segregating for female mating preferences and male colour dissociated from other species differences by breeding hybrids between species of the cichlid fish genus Pundamilia. We measured male mating success as a function of male colour. First, we demonstrate that non-hybrid females of both species use male nuptial coloration for choosing mates, but with inversed preferences. Second, we show that variation in female mating preferences in an F2 hybrid population generates a quadratic fitness function for male coloration suggestive of disruptive selection: intermediate males obtained fewer matings than males at either extreme of the colour range. If the genetics of female mate choice in Pundamilia are representative for those in other species of Lake Victoria cichlid fish, it may help explain the origin and maintenance of phenotypic diversity despite some gene flow.     

Sexual selection in an anadromous population of threespine sticklebacks — no role for parasites

Summary We examined the hypothesis that trematode parasites played a role in the evolution of the red colour of male threespine sticklebacks (Gasterosteus aculeatus L.) and whether the parasites affected female fitness. Parasites (blackspot disease) played no role either in determining the outcome of male—male competition for breeding territories or in female mate choice. Among males with territories, mating success was highly variable. Some males obtained over 3000 eggs (approximately 10 matings) whereas others received none. In 1 year of the 2 year study, males with the greatest amount of red nuptial coloration had the greatest mating success. Although male colour may sometimes affect female choice in this system, this preference has probably not evolved because of the Hamilton—Zuk mechanism of sexual selection. The parasites had small, but statistically significant effects on female fitness. Females with high parasite loads were in poorer condition and produced fewer eggs than less parasitized fish.     

Effects of a parasitic nematode on male mate choice in a livebearing fish with a coercive mating system (western mosquitofish, Gambusia affinis)

I examined the effects of the parasitic larval nematode, Eustrongylides ignotus, on male mate choice in the western mosquitofish, Gambusia affinis. I hypothesized that parasite presence influences male mate choice either directly (via reduction in male mating behavior due to presence of parasite in females) or indirectly (via reduction in male mating behavior due to reduced condition of infected females). Specifically, I tested the predictions that (1) males would mate preferentially with uninfected over infected females (scoring both mating attempts and association time with females); (2) parasitized females would be in poorer condition than non-parasitized females (measured as soluble fat stores); and (3) parasitized females would have reduced fecundity (measured as number of developing embryos). Males preferred to mate with non-parasitized over parasitized females, but showed no differences in association time between females. The nematode did not decrease female body condition, but did decrease female mass, and appeared to decrease female fecundity via reduction in broods (# embryos). Results support that parasites affect male mate choice in mosquitofish; however, the mechanisms used by males to differentiate between parasitized and non-parasitized females remain untested. This study provides the first empirical evidence of parasite affects on male mate choice in livebearing fishes, and suggest a potentially important role for parasite-mediated sexual selection in organisms that use coercive mating as the primary mechanism of obtaining mates.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.     

Predictors of male insemination success in the mosquitofish (Gambusia holbrooki)

Identifying targets of selection is key to understanding the evolution of sexually selected behavioral and morphological traits. Many animals have coercive mating, yet little is known about whether and how mate choice operates when these are the dominant mating tactic. Here, we use multivariate selection analysis to examine the direction and shape of selection on male insemination success in the mosquitofish (Gambusia holbrooki). We found direct selection on only one of five measured traits, but correlational selection involving all five traits. Larger males with longer gonopodia and with intermediate sperm counts were more likely to inseminate females than smaller males with shorter gonopodia and extreme sperm counts. Our results highlight the need to investigate sexual selection using a multivariate framework even in species that lack complex sexual signals. Further, female choice appears to be important in driving the evolution of male sexual traits in this species where sexual coercion is the dominant mating tactic.     

Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback

Mating isolation is a frequent contributor to ecological speciation – but how consistently does it evolve as a result of divergent selection? We tested for genetically based mating isolation between lake and stream threespine stickleback (Gasterosteus aculeatus L.) from the Misty watershed, Vancouver Island, British Columbia. We combined several design elements that are uncommon in the studies of stickleback mate choice: (i) we used second‐generation laboratory‐reared fish (to reduce environmental and maternal effects), (ii) we allowed for male–male competitive interactions (instead of the typical no‐choice trials) and (iii) we included hybrids along with pure types. Males of different types (Lake, Inlet, hybrid) were paired in aquaria, allowed to build nests and then exposed sequentially to females of all three types. We found that Lake and Inlet males differed in behaviours thought to influence stickleback mate choice (inter‐ and intra‐sexual aggression, display and nest activities), whereas hybrids were either intermediate or apparently ‘inferior’ in these behaviours. Despite these differences, Lake and Inlet fish did not mate assortatively and hybrid males did not have a mating disadvantage. Our study reinforces the noninevitability of mating isolation evolving in response to ecological differences and highlights the need to further investigate the factors promoting and constraining progress towards ecological speciation.     

Opportunities for mate choice in the fission‐performing ant Cataglyphis cursor

1. Sexual selection has been little studied in social insects. Nonetheless, because mating is generally for life, opportunities for selecting among mating partners should be exploited. 2. In some ants, males aggregate at nest entrances to mate with emerging gynes. Both males and females thus have access to multiple mates over a relatively protracted period, giving rise to opportunities for mate choice and multiple mating. 3. We provide data from field observations of the male mating biology of the ant, Cataglyphis cursor Fonscolombe. In this species, females mate with, on average, six males each at the nest entrance and found colonies with the help of workers. 4. Males were present at the field site for approximately 1 month in spring, with up to 40 males at a single nest entrance for, on average, 4.7 days. Individual males were observed to survive up to 3 days, and mate up to eight times. 5. Thus both males and females of this species have the ability to mate multiply and have a window permitting mate choice to occur. Workers actively attacked males and may take part in the mate choice process, making C. cursor an interesting model to study questions relating to sexual selection and male mating strategies.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

Is bigger better? Male body size affects wing‐borne courtship signals and mating success in the olive fruit fly,Bactrocera oleae (Diptera: Tephritidae)

Variations in male body size are known to affect inter‐ and intrasexual selection outcomes in a wide range of animals. In mating systems involving sexual signaling before mating, body size often acts as a key factor affecting signal strength and mate choice. We evaluated the effect of male size on courtship displays and mating success of the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae). Wing vibrations performed during successful and unsuccessful courtships by large and small males were recorded by high‐speed videos and analyzed through frame‐by‐frame analysis. Mating success of large and small males was investigated. The effect of male–male competition on mating success was evaluated. Male body size affected both male courtship signals and mating outcomes. Successful males showed wing‐borne signals with high frequencies and short interpulse intervals. Wing vibrations displayed by successful large males during copulation attempt had higher frequencies over smaller males and unsuccessful large males. In no‐competition conditions, large males achieved higher mating success with respect to smaller ones. Allowing large and small males to compete for a female, large males achieve more mating success over smaller ones. Mate choice by females may be based on selection of the larger males, able to produce high‐frequency wing vibrations. Such traits may be indicative of “good genes,” which under sexual selection could means good social‐interaction genes, or a good competitive manipulator of conspecifics.     

Mate Choice in Experimentally Parasitized Rock Doves: Lousy Males Lose

A recent model by Hamilton and Zuk (1982) suggests that exaggeratedsecondary sexual traits facilitate mate choice for genetic resistanceto parasites. The model predicts that individuals discriminateagainst parasitized mates by scrutinizing traits indicativeof parasite load. In the case of birds and their feather-feedinglice, for example, individuals might avoid parasitized matesbydetecting reduced plumage brightness, reduced courtship display,or increased grooming. I conducted a series of mate choice trialsin which female Rock Doves (Columba livia) were allowed to choosebetween "clean" males without lice and "lousy" males with experimentallyincreased loads. Clean males displayed significantly more oftenthan lousy males and females demonstrated a significant preferencefor clean males. Lousy males were subject to plumage damage;however, none of the damage was externally visible, and thetime spent grooming by clean and lousy males did not differsignificantly. Female louse loads, which were also manipulated,were not significantly related to female mating preferences.These results are consistent with the Hamilton-Zuk model. Theyare also consistent with a model of sexual selection for theavoidance of parasite transmission, which is discussed. Thegeneral relevance of lice and other ectoparasites to modelsof parasite-mediated sexual selection is reviewed.