In the surf zone: Reproductive strategy of the calico surfperch (Amphistichus koelzi) in a comparative context

We examined the reproductive life history of calico surfperch (Amphistichus koelzi), including mating season, pregnancy, gestation and multiple paternity utilizing restriction site-associated DNA sequencing. Furthermore, we compared the mating season of calico with barred (Amphistichus argenteus), walleye (Hyperprosopon argenteum) and silver (Hyperprosopon ellipticum) surfperches to determine if the timing of reproduction is divergent within and between the genera. In calico surfperch, the mating season occurs from October to November, and females gestate from December to May. All broods exhibit multiple paternity with a range of four to seven sires per brood. The mating season of calico overlaps completely with barred surfperch; however, barred surfperches have a protracted mating season which extends until the beginning of December, which may be due to differences in reproductive strategy such as size at first reproduction. In the genus, the Hyperprosopon mating season begins earlier than Amphistichus, with divergence in the onset of mating between Hyperprosopon congeners of approximately 1 month.     

Benefits of polyandry: Molecular evidence from field‐caught dung beetles

When females mate with multiple males, they set the stage for postcopulatory sexual selection via sperm competition and/or cryptic female choice. Surprisingly little is known about the rates of multiple mating by females in the wild, despite the importance of this information in understanding the potential for postcopulatory sexual selection to drive the evolution of reproductive behaviour, morphology and physiology. Dung beetles in the genus Onthophagus have become a laboratory model for studying pre‐ and postcopulatory sexual selection, yet we still lack information about the reproductive behaviour of female dung beetles in natural populations. Here, we develop microsatellite markers for Onthophagus taurus and use them to genotype the offspring of wild‐caught females and to estimate natural rates of multiple mating and patterns of sperm utilization. We found that O. taurus females are highly polyandrous: 88% of females produced clutches sired by at least two males, and 5% produced clutches with as many as five sires. Several females (23%) produced clutches with significant paternity skew, indicating the potential for strong postcopulatory sexual selection in natural populations. There were also strong positive correlations between the number of offspring produced and both number of fathers and paternity skew, which suggests that females benefit from mating polyandrously by inciting postcopulatory mechanisms that bias paternity towards males that can sire more viable offspring. This study evaluates the fitness consequences of polyandry for an insect in the wild and provides strong evidence that female dung beetles benefit from multiple mating under natural conditions.     

Genetic evidence for the mating system and reproductive success of black sea bream (Acanthopagrus schlegelii)

Understanding the mating system and reproductive success of a species provides evidence for sexual selection. We examined the mating system and the reproductive success of captive adult black sea bream (Acanthopagrus schlegelii), using parentage assignment based on two microsatellites multiplex PCR systems, with 91.5% accuracy in a mixed family (29 sires, 25 dams, and 200 offspring). Based on the parentage result, we found that 93.1% of males and 100% of females participated in reproduction. A total of 79% of males and 92% of females mated with multiple partners (only 1 sire and 1 dam were monogamous), indicating that polygynandry best described the genetic mating system of black sea bream. For males, maximizing the reproductive success by multiple mating was accorded with the sexual selection theory while the material benefits hypothesis may contribute to explain the multiple mating for females. For both sexes, there was a significant correlation between mating success and reproductive success and the variance in reproductive success of males was higher than females. Variation in mating success is the greatest determinant to variation in reproductive success when the relationship is strongly positive. The opportunity for sexual selection of males was twice that of females, as well as the higher slope of the Bateman curve in males suggested that the intensity of intrasexual selection of males was higher than females. Thus, male–male competition would lead to the greater variation of mating success for males, which caused greater variation in reproductive success in males. The effective population number of breeders (N_b) was 33, and the N_b/N ratio was 0.61, slightly higher than the general ratio in polygynandrous fish populations which possibly because most individuals mated and had offspring with a low variance. The relatively high N_b contributes to the maintenance of genetic diversity in farmed black sea bream populations.     

Paternity analyses in wild‐caught and laboratory‐reared Caribbean cricket females reveal the influence of mating environment on post‐copulatory sexual selection

Polyandry is ubiquitous in insects and provides the conditions necessary for male‐ and female‐driven forms of post‐copulatory sexual selection to arise. Populations of Amphiacusta sanctaecrucis exhibit significant divergence in portions of the male genitalia that are inserted directly into the female reproductive tract, suggesting that males may exercise some post‐copulatory control over fertilization success. We examine the potential for male–male and male–female post‐copulatory interactions to influence paternity in wild‐caught females of A. sanctaecrucis and contrast our findings with those obtained from females reared in a high‐density laboratory environment. We find that female A. sanctaecrucis exercise control by mating multiple times (females mount males), but that male–male post‐copulatory interactions may influence paternity success. Moreover, post‐copulatory interactions that affect reproductive success of males are not independent of mating environment: clutches of wild‐caught females exhibit higher sire diversity and lower paternity skew than clutches of laboratory‐reared females. There was no strong evidence for last male precedence in either case. Most attempts at disentangling the contributions of male–male and male–female interactions towards post‐copulatory sexual selection have been undertaken in a laboratory setting and may not capture the full context in which they take place – such as the relationship between premating and post‐mating interactions. Our results reinforce the importance of designing studies that can capture the multifaceted nature of sexual selection for elucidating the role of post‐copulatory sexual selection in driving the evolution of male and female reproductive traits, especially when different components (e.g. precopulatory and post‐copulatory interactions) do not exert independent effects on reproductive outcomes.     

Multiple paternity in a wild population of Armadillidium vulgare: influence of infection with Wolbachia?

Female multiple mating has been extensively studied to understand how nonobvious benefits, generally thought to be of genetic nature, could overcome heavy costs such as an increased risk of infection during mating. However, the impact of infection itself on multiple mating has rarely been addressed. The interaction between the bacterium Wolbachia and its terrestrial crustacean host, Armadillidium vulgare, is a relevant model to investigate this question. In this association, Wolbachia is able to turn genetic males into functional females (i.e. feminization), thereby distorting the sex ratio and decreasing the number of available males at the population scale. Moreover, in A. vulgare, females have been shown to mate multiply under laboratory conditions and males prefer uninfected females over infected ones. Additionally, different Wolbachia strains are known to infect A. vulgare and these strains differ in their transmission rate and virulence. All these elements suggest a potential impact of different Wolbachia strains on multiple mating. To investigate this assumption, we collected gravid females in a wild A. vulgare population harbouring both uninfected females and females infected with one of two different Wolbachia strains (wVulM and wVulC) and performed paternity analyses on the obtained broods using microsatellite markers. We demonstrate that (i) multiple paternity is common in this wild population of A. vulgare, with a mean number of fathers of 4.48 ± 1.24 per brood and (ii) females infected with wVulC produced broods with a lower multiple paternity level compared with females infected with wVulM and uninfected ones. This work improves our knowledge of the impact of infections on reproductive strategies.     

The measure and significance of Bateman's principles

Bateman''s principles explain sex roles and sexual dimorphism through sex-specific variance in mating success, reproductive success and their relationships within sexes (Bateman gradients). Empirical tests of these principles, however, have come under intense scrutiny. Here, we experimentally show that in replicate groups of red junglefowl, Gallus gallus, mating and reproductive successes were more variable in males than in females, resulting in a steeper male Bateman gradient, consistent with Bateman''s principles. However, we use novel quantitative techniques to reveal that current methods typically overestimate Bateman''s principles because they (i) infer mating success indirectly from offspring parentage, and thus miss matings that fail to result in fertilization, and (ii) measure Bateman gradients through the univariate regression of reproductive over mating success, without considering the substantial influence of other components of male reproductive success, namely female fecundity and paternity share. We also find a significant female Bateman gradient but show that this likely emerges as spurious consequences of male preference for fecund females, emphasizing the need for experimental approaches to establish the causal relationship between reproductive and mating success. While providing qualitative support for Bateman''s principles, our study demonstrates how current approaches can generate a misleading view of sex differences and roles.     

Female mate choice predicts paternity success in the absence of additive genetic variance for other female paternity bias mechanisms in Drosophila serrata

After choosing a first mate, polyandrous females have access to a range of opportunities to bias paternity, such as repeating matings with the preferred male, facilitating fertilization from the best sperm or differentially investing in offspring according to their sire. Female ability to bias paternity after a first mating has been demonstrated in a few species, but unambiguous evidence remains limited by the access to complex behaviours, sperm storage organs and fertilization processes within females. Even when found at the phenotypic level, the potential evolution of any mechanism allowing females to bias paternity other than mate choice remains little explored. Using a large population of pedigreed females, we developed a simple test to determine whether there is additive genetic variation in female ability to bias paternity after a first, chosen, mating. We applied this method in the highly polyandrous Drosophila serrata, giving females the opportunity to successively mate with two males ad libitum. We found that despite high levels of polyandry (females mated more than once per day), the first mate choice was a significant predictor of male total reproductive success. Importantly, there was no detectable genetic variance in female ability to bias paternity beyond mate choice. Therefore, whether or not females can bias paternity before or after copulation, their role on the evolution of sexual male traits is likely to be limited to their first mate choice in D. serrata.     

The Consequences of Predation Risk on the Male Territorial Behavior in a Solitary Bee

Territorial males may adopt a mating tactic that yields greater reproductive success but that at the same time increases the risk of predation. Plasticity in reproductive behavior can reflect a balance between sexual selection and natural selection. In this study, we sought to verify the effect of predation risk on territorial behavior of males of the solitary bee Ptilothrix fructifera (Apidae). Males of the species employ alternative mating tactics and can be territorial in defense of larval food sources. By manipulating predator models in the field, we tested whether (1) males avoid perch flowers containing predator models; (2) males alternate between mating tactics when their territory is associated with a predation risk; and (3) female foraging on flowers in a territory is altered in the presence of a predator model. We measured the responses of males and females in flowers containing and not containing a model of a spider or a stuffed bird. The results show that territorial males of P. fructifera alter their territorial behavior when faced with a high risk of predation. They do not abandon their territory or change to a non‐territorial mating tactic, but instead change the use of their territory, avoiding flowers containing predator models or perching on other flowers when the previous flower presented a potential predation risk. Female P. fructifera decreases the frequency of their visits to flowers and the length of time spent there in the presence of a spider model. In short, in the face of predation risk, females and males alter their behaviors at the cost of less efficient foraging and searching for partners, respectively.     

High levels of polyandry,but limited evidence for multiple paternity,in wild populations of the western rock lobster (Panulirus cygnus)

Polyandry, where multiple mating by females results in the temporal and spatial overlap of ejaculates from two or more males, is taxonomically widespread and occurs in varying frequencies within and among species. In decapods (crabs, lobsters, crayfish, and prawns), rates of polyandry are likely to be variable, but the extent to which patterns of multiple paternity reflect multiple mating, and thus are shaped by postmating processes that bias fertilization toward one or a subset of mated males, is unclear. Here, we use microsatellite markers to examine the frequency of multiple mating (the presence of spermatophores from two or more males) and patterns of paternity in wild populations of western rock lobster (Panulirus cygnus). Our data confirm that >45% of females had attached spermatophores arising from at least two males (i.e., confirming polyandry), but we found very limited evidence for multiple paternity; among 24 clutches sampled in this study, only two arose from fertilizations by two or more males. Single inferred paternal genotypes accounted for all remaining progeny genotypes in each clutch, including several instances when the mother had been shown to mate with two or more males. These findings highlight the need for further work to understand whether polyandry is adaptive and to uncover the mechanisms underlying postmating paternity biases in this system.     

The impact of Wolbachia,male age and mating history on cytoplasmic incompatibility and sperm transfer in Drosophila simulans

Most insects harbour a variety of maternally inherited endosymbionts, the most widespread being Wolbachia pipientis that commonly induce cytoplasmic incompatibility (CI) and reduced hatching success in crosses between infected males and uninfected females. High temperature and increasing male age are known to reduce the level of CI in a variety of insects. In Drosophila simulans, infected males have been shown to mate at a higher rate than uninfected males. By examining the impact of mating rate independent of age, this study investigates whether a high mating rate confers an advantage to infected males through restoring their compatibility with uninfected females over and above the effect of age. The impact of Wolbachia infection, male mating rate and age on the number of sperm transferred to females during copulation and how it relates to CI expression was also assessed. As predicted, we found that reproductive compatibility was restored faster in males that mate at higher rate than that of low mating and virgin males, and that the effect of mating history was over and above the effect of male age. Nonvirgin infected males transferred fewer sperm than uninfected males during copulation, and mating at a high rate resulted in the transfer of fewer sperm per mating irrespective of infection status. These results indicate that the advantage to infected males of mating at a high rate is through restoration of reproductive compatibility with uninfected females, whereas uninfected males appear to trade off the number of sperm transferred per mating with female encounter rate and success in sperm competition. This study highlights the importance Wolbachia may play in sexual selection by affecting male reproductive strategies.     

Increase in multiple paternity across the reproductive lifespan in a sperm‐storing,hermaphroditic freshwater snail

Polyandry is a common phenomenon and challenges the traditional view of stronger sexual selection in males than in females. In simultaneous hermaphrodites, the physical proximity of both sex functions was long thought to preclude the operation of sexual selection. Laboratory studies suggest that multiple mating and polyandry in hermaphrodites may actually be common, but data from natural populations are sparse. We therefore estimated the rate of multiple paternity and its seasonal variability in the annual, sperm‐storing, simultaneously hermaphroditic freshwater snail Radix balthica for the entire duration of the reproductive lifespan. We also tested whether multiple paternity was associated with clutch size or embryonic development. To obtain these data, we measured and genotyped 60 field‐collected egg clutches using nine highly polymorphic microsatellite markers. Overall, 50% of the clutches had multiple fathers, and both the frequency (20–93% of clutches) and magnitude of multiple paternity (mean 1.3–3.8 fathers per clutch) substantially increased over time, probably because of extensive sperm storage. Most multiply sired clutches (83%) had a dominant father, but neither clutch size nor the proportion of developed embryos per clutch was associated with levels of multiple paternity. Both the evident promiscuity and the frequent skew of paternity shares suggest that sexual selection may be an important evolutionary force in the study population.     

EFFECTS OF SOCIAL AND EXTRA‐PAIR MATING ON SEXUAL SELECTION IN BLUE TITS (CYANISTES CAERULEUS)

The contribution of extra‐pair paternity (EPP) to sexual selection has received considerable attention, particularly in socially monogamous species. However, the importance of EPP remains difficult to assess quantitatively, especially when many extra‐pair young have unknown sires. Here, we combine measurements of the opportunity for selection (I), the opportunity for sexual selection (I_S), and the strength of selection on mating success (Bateman gradient, β_SS) with a novel simulation of random mating tailored to the specific mating system of the blue tit (Cyanistes caeruleus). In a population where social polygyny and EPP are common, the opportunity for sexual selection was significantly stronger and Bateman gradients significantly steeper for resident males than for females. In general, success with the social mate(s) contributed most to variation in male reproductive success. Effects of EPP were small, but significantly higher than expected under random mating. We used sibship analysis to estimate the number of unknown sires in our population. Under the assumption that the unknown sires are nonbreeding males, EPP reduced the variance in and the strength of selection on mating success, a possibility that hitherto has not been considered.     

Polyandrous females produce sons that are successful at post‐copulatory competition

Some of the genetic benefit hypotheses put forward to explain multiple male mating (polyandry) predict that sons of polyandrous females will have an increased competitive ability under precopulatory or post‐copulatory competition via paternally inherited traits, such as attractiveness or fertilization efficiency. Here, we tested these predictions by comparing the competitive ability of sons of experimentally monandrous and polyandrous female bank voles (Myodes glareolus), while controlling for potential material and maternal effects. In female choice experiments, we found no clear preference for sons of either monandrous or polyandrous mothers. Moreover, neither male type was dominant over the other, indicating no advantage in precopulatory male contest competition. However, in competitive matings, sons of polyandrous mothers significantly increased their mating efforts (mating duration, intromission number). In line with this, paternity success was biased towards sons of polyandrous mothers. Because there was no evidence for maternal effects, our results suggest that female bank voles gain genetic benefits from polyandry.     

Females of the Cellar Spider Discriminate Against Previous Mates

Mate choice for novel partners should evolve when remating with males of varying genetic quality provides females with fitness‐enhancing benefits. We investigated sequential mate choice for same or novel mating partners in females of the cellar spider Pholcus phalangioides (Pholcidae) to understand what drives female remating in this system. Pholcus phalangioides females are moderately polyandrous and show reluctance to remating, but double‐mated females benefit from a higher oviposition probability compared to single‐mated females. We exposed mated females to either their former (same male) or a novel mating partner and assessed mating success together with courtship and copulatory behaviours in both sexes. We found clear evidence for mate discrimination: females experienced three‐fold higher remating probabilities with novel males, being more often aggressive towards former males and accepting novel males faster in the second than in the first mating trial. The preference for novel males suggests that remating is driven by benefits derived from multiple partners. The low remating rates and the strong last male sperm precedence in this system suggest that mating with novel partners that represent alternative genotypes may be a means for selecting against a former mate of lower quality.     

Male burying beetles extend,not reduce,parental care duration when reproductive competition is high

Male parents spend less time caring than females in many species with biparental care. The traditional explanation for this pattern is that males have lower confidence of parentage, so they desert earlier in favour of pursuing other mating opportunities. However, one recent alternative hypothesis is that prolonged male parental care might also evolve if staying to care actively improves paternity. If this is the case, an increase in reproductive competition should be associated with increased paternal care. To test this prediction, we manipulated the level of reproductive competition experienced by burying beetles, Nicrophorus vespilloides (Herbst, 1783). We found that caregiving males stayed for longer and mated more frequently with their partner when reproductive competition was greater. Reproductive productivity did not increase when males extended care. Our findings provide support for the increased paternity hypothesis. Extended duration of parental care may be a male tactic both protecting investment (in the current brood) and maximizing paternity (in subsequent brood(s) via female stored sperm) even if this fails to maximize current reproductive productivity and creates conflict of interest with their mate via costs associated with increased mating frequency.     

Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon)

We used data collected over 3 years at two study sites to quantifythe rates and consequences of multiple paternity and to determinethe opportunity for selection on male and female northern watersnakes (Nerodia sipedon). We sampled litters from 45 femalesthat gave birth to 811 offspring. Using eight microsatelliteDNA loci (probability of exclusion of nonparental males >0.99), we assigned paternity to 93% of neonates from one studypopulation and 69% of neonates from the other population. Observationsof participation in mating aggregations predicted individual reproductive success poorly for two reasons. First, males regularlycourted nonreproductive females. Second, more than half ofall sexually mature males obtained no reproductive successeach year, despite the fact that many of them participatedin mating aggregations. The number of sires per litter ranged from one to five, with 58% of all litters sired by more thanone male. Multiple paternity increased with female size, apparentlyboth because bigger females mated with more males and becausethe larger litters of big females provide paternity opportunitiesto more males. Multiple paternity was also more prevalent inyears with shorter mating seasons. We detected no advantage to multiple paternity in reducing either the number of unfertilizedovules or stillborn young. Despite the majority of males siringno young each year, some males fathered young with as manyas three different females in one year. Male reproductive successincreased by more than 10 offspring for each additional mate,whereas female success increased by fewer than 2 offspring foreach additional mate. The opportunity for sexual selectionwas more than five times higher in males than females.     

Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.     

Pollinator identity and spatial isolation influence multiple paternity in an annual plant

The occurrence and extent of multiple paternity is an important component of variation in plant mating dynamics. However, links between pollinator activity and multiple paternity are generally lacking, especially for plant species that attract functionally diverse floral visitors. In this study, we separated the influence of two functionally distinct floral visitors (hawkmoths and solitary bees) and characterized their impacts on multiple paternity in a self‐incompatible, annual forb, Oenothera harringtonii (Onagraceae). We also situated pollinator‐mediated effects in a spatial context by linking variation in multiple paternity to variation in plant spatial isolation. We documented pronounced differences in the number of paternal sires as function of pollinator identity: on average, the primary pollinator (hawkmoths) facilitated mating with nearly twice as many pollen donors relative to the secondary pollinator (solitary bees). This effect was consistent for both isolated and nonisolated individuals, but spatial isolation imposed pronounced reductions on multiple paternity regardless of pollinator identity. Considering that pollinator abundance and pollen dispersal distance did not vary significantly with pollinator identity, we attribute variation in realized mating dynamics primarily to differences in pollinator morphology and behaviour as opposed to pollinator abundance or mating incompatibility arising from underlying spatial genetic structure. Our findings demonstrate that functionally distinct pollinators can have strongly divergent effects on polyandry in plants and further suggest that both pollinator identity and spatial heterogeneity have important roles in plant mating dynamics.     

Multiple paternity and competition in sympatric congeneric reef fishes, Embiotoca jacksoni and E. lateralis

The black surfperch Embiotoca jacksoni and the striped surfperch E. lateralis (Embiotocidae, Perciformes) are livebearing temperate reef fishes that live sympatrically over a large portion of their distribution range, where they exhibit strong ecological competition. In order to assess whether mating strategies reflect competition, we investigated multiple paternity in these two species in an area of sympatry. We sampled 24 pregnant females (12 for each species) in Monterey Bay, California, used microsatellite analysis and assessed paternity with the COLONY software. While broods are relatively small (12 to 36 offspring), they were always sired by multiple fathers (2 to 9), with no correlation between the size of a brood and the number of fathers. The number of sires for each brood was not significantly different between the two species (approximately 3.5 sires per brood). We tested the deviation from stochasticity of fathered offspring for each father in one brood. Results showed a significant deviation for both E. jacksoni and E. lateralis . However, this deviation was not found to be significant between species. The striking similarity in the dynamics of multiple paternity in these species, when sampled in sympatry, may result from several alternative scenarios, including phylogenetic inertia, reproductive behaviour, and ecological competition.     

Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection

Sexual selection theory posits that ornamental traits can evolve if they provide individuals with an advantage in securing multiple mates. That male ornamentation occurs in many bird species in which males pair with a single female is therefore puzzling. It has been proposed that extra-pair mating can substantially increase the variance in reproductive success among males in monogamous species, thus increasing the potential for sexual selection. We documented the frequency of extra-pair paternity and examined its effect on variation in male reproductive success in the mountain bluebird Sialia currucoides , a socially monogamous songbird in which males possess brilliant plumage ornamentation. Extra-pair paternity was common in our Wyoming study population, with 72% of broods containing at least one extra-pair offspring. The standardized variance in actual male reproductive success (i.e., the total number of within-pair and extra-pair offspring sired) was more than seven times higher than the variation in apparent success (i.e., success assuming that no extra-pair mating occurred). Success at siring within-pair and extra-pair offspring both contributed to the variation in overall male reproductive success. Within-pair success, however, did not predict a male's level of extra-pair success, suggesting that males do not sacrifice within-pair paternity to gain extra-pair paternity. Calculation of the sexual selection (Bateman) gradient showed that males sire approximately two additional offspring for each extra-pair mate that we identified. Thus, in this sexually dichromatic species, extra-pair mating increases the variance in male reproductive success and provides the potential for sexual selection to act.