Experimental Removal of Sexual Selection Reveals Adaptations to Polyandry in Both Sexes

Polyandrous mating is extremely common, yet for many species the evolutionary significance is not fully resolved. In order to understand the evolution of mating systems, it is crucial that we investigate the adaptive consequences across many facets of reproduction. We performed experimental evolution with the naturally polygamous flour beetle Tribolium castaneum subjected to either polyandry or enforced monogamy, creating contrasting selection regimes associated with the presence or absence of sexual selection. After 36 generations, we investigated male and female adaptations by mating beetles with an unselected tester strain to exclude potential effects of male–female coevolution. Reproductive success of focal monogamous and polyandrous beetles from each sex was assessed in separate single male and multiple male experiments emulating the different selection backgrounds. Males and females from the polyandrous regime had more offspring in the experiments with multiple males present than monogamous counterparts. However, in single male experiments, neither females nor males differed between selection regimes. Subsequent mating trials with multiple males suggested that adaptations to polyandry in both sexes provide benefits when choice and competition were allowed to take place. Polyandrous females delayed the first copulation when given a choice of males and polyandrous males were quicker to achieve copulation when facing competition. In conclusion, we show that the expected benefits of evolutionary adaptation to polyandry in T. castaneum depended on the availability of multiple mates. This context-dependent effect, which concerned both sexes, highlights the importance of realistic competition and choice experiments.     

Male age and sexual experience affect male mating behavior in the hawthorn spider mite,Amphitetranychus viennensis

As is reported, in species with first-male sperm precedence, male age and previous sexual experience play crucial roles in male mating behavior. In the hawthorn spider mite, Amphitetranychus viennensis Zacher, previous studies showed that only females that copulated for the first time could achieve fertilization. Based on this, the effects of male age and mating history on male mate choice and male mate competition were investigated. It was confirmed that males could distinguish virgins from fertilized females but they were unable to discriminate between virgins and unfertilized females. Interestingly, the copulation duration of males mated with fertilized females was much shorter than that of males mated with virgins or unfertilized females. Additionally, for male mating choice, males of all ages and more experienced males preferred 5-day-old virgin females, whereas only less experienced males preferred 1-day-old virgin females. In male-male competition, 3-day-old males were more competitive and obtained more copulations compared with others. Copula duration was closely related to male age. Though no significant differences were observed in mating competition between virgin and mated males, copula duration of males in first copulation was the longest and gradually shortened in subsequent copulations. In all, this investigation demonstrated that male age and sexual experience affected male mate choice and male-male competition, leading to further insight into the influences of male age and sexual experience on the reproductive fitness of both sexes.

     

The effect of mating frequency and mating pattern on female reproductive fitness in cabbage beetle,Colaphellus bowringi

It is generally thought that females can receive more of the material benefits from males by increasing mating frequency and polyandry can lead to greater reproductive success. The cabbage beetle, Colaphellus bowringi Baly (Coleoptera: Chrysomelidae), is a highly promiscuous species, in which females or males can readily mate repeatedly with a given partner or multiple partners at a very high frequency. In the present study, the effect of mating frequency (number of matings) and mating pattern (polyandry vs. monogamy) on female reproductive fitness was investigated by measuring fecundity, fertility, and female longevity. The results indicated that increased female mating frequency with the same male did not result in variation in lifetime fecundity, but significantly increased fertility and decreased female longevity. Moreover, five copulations were sufficient to acquire maximal reproductive potential. Female lifetime fecundity also did not differ between polyandrous and monogamous treatments. However, monogamous females exhibited a significant increase in fertility and significant prolongation of longevity compared with polyandrous females, further demonstrating that monogamy is superior to polyandry in this beetle.     

Polyandrous females provide sons with more competitive sperm: Support for the sexy‐sperm hypothesis in the rattlebox moth (Utetheisa ornatrix)

Given the costs of multiple mating, why has female polyandry evolved? Utetheisa ornatrix moths are well suited for studying multiple mating in females because females are highly polyandrous over their life span, with each male mate transferring a substantial spermatophore with both genetic and nongenetic material. The accumulation of resources might explain the prevalence of polyandry in this species, but another, not mutually exclusive, possibility is that females mate multiply to increase the probability that their sons will inherit more‐competitive sperm. This latter “sexy‐sperm” hypothesis posits that female multiple mating and male sperm competitiveness coevolve via a Fisherian runaway process. We tested the sexy‐sperm hypothesis by using competitive double matings to compare the sperm competition success of sons of polyandrous versus monandrous females. In accordance with sexy‐sperm theory, we found that in 511 offspring across 17 families, the male whose polyandrous mother mated once with each of three different males sired significantly more of all total offspring (81%) than did the male whose monandrous mother was mated thrice to a single male. Interestingly, sons of polyandrous mothers had a significantly biased sex ratio of their brood toward sons, also in support of the hypothesis.     

Paternity costs from polyandry compensated by increased fecundity in the hide beetle

Polyandry-induced sperm competition is assumed to impose costson males through reduced per capita paternity success. In contrast,studies focusing on the consequences of polyandry for femalesreport increased oviposition rates and fertility. For thesespecies, there is potential for the increased female fecundityassociated with polyandry to offset the costs to males of sharedpaternity. We tested this hypothesis by comparing the proportionand number of offspring sired by males mated with monandrousand polyandrous females in the hide beetle, Dermestes maculates,both for males mating with different females and for males rematingwith the same female. In 4 mating treatments, monandrous femalesmated either once or twice with the same male and polyandrousfemales mated either twice with 2 different males or thricewith 2 males (where 1 male mated twice). Polyandrous and twice-matingmonandrous females displayed greater fecundity and fertilitythan singly mating monandrous females. Moreover, males rematedto the same female had greater paternity regardless of whetherthat female mated with another male. In both polyandrous treatments,male mating order did not affect paternity success. Finally,although the proportion of eggs sired decreased if a male matedwith a polyandrous female, multiply mating females or femalesthat remated with a previous mate laid significantly more eggsand thus the actual number of eggs sired was comparable. Thus,males do not necessarily accrue a net fitness loss when matingwith polyandrous females. This may explain the absence of anyobvious defensive paternity-protection traits in hide beetlesand other species.     

Can females gain extra paternal investment by mating with multiple males? A game theoretic approach

Although females may require only one mating to become inseminated, many female animals engage in costly mating with multiple males. One potential benefit of polyandrous mating is gaining parental investment from multiple males. We developed two game theoretic models to explore this possibility. Our first model showed that male care of multiple females' offspring evolves when male help substantially increases offspring fitness, future mating opportunity is limited, and group size is small. In our second model, we assumed that males invest in the offspring of former mates and evaluated the fitness consequences of female monogamous and polyandrous mating strategies. Females benefit only from limited polyandry, that is, mating with several males. Polyandry is discouraged because females must share male investment with other polyandrous females, and paternal care is likely to experience diminishing returns. Females may enhance their access to male investment by competing with rival females and monopolizing investment, however. The results support the argument that females can gain paternal investment by mating with several males in small social groups (e.g., dunnocks Prunella modularis). The results do not support the argument that females can gain paternal investment from pronounced multiple mating in large social groups, however, as observed in many primate species.     

Polyandry promotes enhanced offspring survival in decorated crickets

Although female multiple mating is ubiquitous in insects, its adaptive significance remains poorly understood. Benefits to multiple mating can accrue via direct material benefits, indirect genetic benefits, or both. We investigated the effects of multiple mating in the decorated cricket, Gryllodes sigillatus, by simultaneously varying the number of times that females mated and the number of different males with which they mated, measuring aspects of female fecundity and elements of offspring performance and viability. Multiple matings resulted in enhanced female fitness relative to single matings when females mated with different partners, but not when females mated repeatedly with the same male. Specifically, polyandrous females produced significantly more offspring surviving to reproductive maturity than did monogamous females mating once or mating repeatedly with the same male. These results suggest that the benefit females gain from multiple mating is influenced primarily by genetic and not material benefits.     

Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

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.     

Parental care and social mating system in the Lesser Spotted Woodpecker Dendrocopos minor

The sexes’ share in parental care and the social mating system in a marked population of the single‐brooded Lesser Spotted Woodpecker Dendrocopos minor were studied in 17 woodpecker territories in southern Sweden during 10 years. The birds showed a very strong mate fidelity between years; the divorce rate was 3.4%. In monogamous pairs, the male provided more parental care than the female. The male did most of the nest building and all incubation and brooding at night. Daytime incubation and brooding were shared equally by the sexes, and biparental care at these early breeding stages is probably necessary for successful breeding. In 42% of the nests, however, though still alive the female deserted the brood the last week of the nestling period, whereas the male invariably fed until fledging and fully compensated for the absent female. Post‐fledging care could not be quantified, but was likely shared by both parents. Females who ceased feeding at the late nestling stage resumed care after fledging. We argue that the high premium on breeding with the same mate for consecutive years and the overall lower survival of females have shaped this male‐biased organisation of parental care. In the six years with best data, most social matings were monogamous, but 8.5% of the females (N=59) exhibited simultaneous multi‐nest (classical) polyandry and 2.9% of the males (N=68) exhibited multi‐nest polygyny. Polyandrous females raised 39% more young than monogamous pairs. These females invested equal amounts of parental care at all their nests, but their investment at each nest was lower than that of monogamous females. The polyandrously mated males fully compensated for this lower female investment. Polygynous males invested mainly in their primary nest and appeared to be less successful than polyandrous females. Polyandry and polygyny occurred only when the population sex ratio was biased, and due to strong intra‐sexual competition this is likely a prerequisite for polygamous mating in Lesser Spotted Woodpeckers.     

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.     

Age,Experience and Sex – Do Female Bulb Mites Prefer Young Mating Partners?

In species where advancing sire age is associated with decreased progeny fitness, female resistance to mating with old partners can be expected to evolve. In polyandrous species, such resistance may be contingent on female mating experience: virgins should be relatively indiscriminate to ensure egg fertility, whereas non‐virgins can be expected to base their re‐mating decisions on the age of their previous versus potential new partners, and ‘trade‐up’ if previously mated with old males. Here, we tested these predictions using a promiscuous and relatively long‐living bulb mite (Rhizoglyphus robini), in which old sire age is associated with decreased fecundity of daughters. In a fully factorial design, we applied two male treatments, young and old, and three female treatments, virgin, previously mated to an old male and previously mated to a young male. Consistent with earlier studies, we observed a reduced mating success of old males. However, we found no support for attributing this result to female discrimination, as female behavior in response to male mounting attempts was not affected by the age of the suitor, or by its interaction with the age of the female’s previous mate. Interestingly, females were passive during 93% of male mounting attempts observed, suggesting that once they are located by a male, they exert little control over copulation. Old males had lower mate‐searching activity and were less efficient in obtaining matings (lower success rate per mounting attempt), suggesting a decreased mate‐securing ability because of aging. Overall, our results suggest that in bulb mites, male ability to secure mates declines with age, whereas they do not support the prediction that females actively discriminate against old partners.     

Copulation patterns in the golden orb-web spider Nephila madagascariensis

A consequence of multiple mating by females can be that the sperm of two or more males directly compete for the fertilisation of ova inside the female reproductive tract. Selection through sperm-competition favours males that protect their sperm against that of rivals and strategically allocate their sperm, e.g., according to the mating status of the female and the morphology of the spermatheca. In the majority of spiders, we encounter the otherwise unusual situation that females possess two independent insemination ducts, both ending in their own sperm storage organ, the spermatheca. Males have paired mating organs, but generally can only fill one spermatheca at a time. We investigated whether males of the African golden orb-web spider Nephila madagascariensis can prevent rival males from mating into the same spermatheca and whether the mating status of the female and/or the spermatheca causes differences in male mating behaviour. There was no significant difference in the duration of copulations into unused spermathecae of virgin and mated females. We found that copulations into previously inseminated spermathecae were generally possible, but shorter than copulations into the unused side of mated females or with virgins. Thus, male N. madagascariensis may have an advantage when they mate with virgins, but cannot prevent future males from mating. However, in rare instances, parts of the male genitals can completely obstruct a female genital opening.     

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.     

The evolution of multiple mating: Costs and benefits of polyandry to females and of polygyny to males

Polyandry is a paradox: why do females mate multiple times when a single ejaculate often provides enough sperm for lifetime egg production? Gowaty et al. addressed explanations for polyandry in Drosophila pseudoobscura from the perspective of hypotheses based on sex differences in costs of reproduction (CoR). Contrary to CoR, Gowaty et al. showed that (1) a single ejaculate was inadequate for lifetime egg production; (2) polyandry provided fitness benefits to females beyond provision of adequate sperm and (3) fitness benefits of polyandry were not offset by costs. Here, I discuss predictions of the ad hoc hypotheses of CoR and three alternative hypotheses to CoR to facilitate a discussion and further development of a strong inference approach to experiments on the adaptive significance of polyandry for females. Each of the hypotheses makes testable predictions; simultaneous tests of the predictions will provide a strong inference approach to understanding the adaptive significance of multiple mating. I describe a sex-symmetric experiment meant to evaluate variation in fitness among lifelong virgins (V); monogamous females and males with one copulation (M_OC); monogamous females and males with multiple copulations (M_MC); P_AND, polyandrous females; and P_GYN, polygynous males. Last, I recommend the study of many different species, while taking care in choice of study species and attention to the assumptions of specific hypotheses. I particularly urge the study of many more Drosophila species both in laboratory and the wild to understand the “nature of flies in nature,” where opportunities and constraints mold evolutionary responses.     

Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae)

The short- and long-term consequences of monogamy and promiscuity in an aphidophagous ladybird, Propylea dissecta (Mulsant) in terms of reproductive performance and offspring fitness were investigated. Promiscuous females were more fecund and laid more viable eggs than monogamous ones. Amongst promiscuous females, those mated with multiple males (freedom for mate choice) had significantly higher reproductive output than those mated daily with a new unmated male. The increased reproductive output of females mated with an unmated male each day in comparison to monogamous ones might possibly be a result of their increased ejaculate size. The further increase in reproductive output, when a female was allowed to choose a mate, may be because of repeated preferential mating with the fitter males. Results on long-term consequences of promiscuity revealed faster development and increased survival in offspring of promiscuous females at 25, 27 and 30 degrees C. The percent adult emergence was more strongly influenced than development by the mating regime. There were no statistically significant differences in survival of offspring of promiscuous females (mate choice) at the three temperatures, while the percent survival of offspring of monogamous females differed significantly. Offspring of promiscuous females (mate choice) were fittest in terms of development and survival, which indicates their probable better genetic constitution and subsequently that of chosen mates. Thus, promiscuity has both short- and long-term benefits and is advantageous to ladybirds. The presence of long-term benefits in terms of fitter offspring probably indicates the evolutionary rationale behind the prevalence of promiscuity in ladybirds.     

Yelling for sex: harem males compete for female access in bronze-winged jacanas

Sperm competition in sex-role reversed, polyandrous jacanas is intense because females copulate with multiple male mates before laying each clutch. These males may be unable to attempt to maximize their share of copulations by mate guarding or forcing copulations. Instead, males in polyandrous harems may compete for sexual access to the female by giving a call, termed the 'yell', to attract her. Male bronze-winged jacanas, Metopidius indicus, yelled at higher rates in larger harems, and when the female was further from the yeller or on a comate's territory. Half of all yells were given at mating platforms where all copulations occurred. Males that received the clutch yelled at lower rates during the incubation and chick care periods. Yells attracted the female when she was far from the yeller or with a comate. When the yell of a polyandrous male was broadcast from his territory, the female was more likely to fly to his territory during playback than during control periods. Within polyandrous harems the males that yelled at the highest rates received the most copulations, and three out of four females gave clutches to the male that gave the longest and most frequent yells, so females may have used yells to assess male quality. Intrusions by females, but not males, increased during yell playbacks, and tended to be more frequent on the territories of males with high yell rates. Females may therefore respond to their mates' yells because yells may attract female intruders which may attempt to take over the territory. Copyright 1999 The Association for the Study of Animal Behaviour.     

A theoretical study on the evolution of male parental care and female multiple mating: effects of female mate choice and male care bias

Male parental care and female multiple mating are seen in many species in spite of the cost they entail. Moreover, they even coexist in some species though polyandry, by reducing paternity confidence of caregiving males, seems to hinder the evolution of paternal care. Previous studies have investigated the coevolutionary process of paternal care and polyandry under various simplifying assumptions, including random mating and random provision of male care. We extend these models to examine possible effects of female mate choice and male care bias, assuming that (a) monandrous females mate preferentially with caregiving males while polyandrous females compromise their preference in order to mate with multiple males and (b) caregiving males tend to direct their care to offspring of monandrous females. Our models suggest that both the female preference and the male bias always favor caregiving males while they may not always facilitate the evolution of monandry.     

Sperm storage mediated by cryptic female choice for nuptial gifts

Polyandrous females are expected to discriminate among males through postcopulatory cryptic mate choice. Yet, there is surprisingly little unequivocal evidence for female-mediated cryptic sperm choice. In species in which nuptial gifts facilitate mating, females may gain indirect benefits through preferential storage of sperm from gift-giving males if the gift signals male quality. We tested this hypothesis in the spider Pisaura mirabilis by quantifying the number of sperm stored in response to copulation with males with or without a nuptial gift, while experimentally controlling copulation duration. We further assessed the effect of gift presence and copulation duration on egg-hatching success in matings with uninterrupted copulations with gift-giving males. We show that females mated to gift-giving males stored more sperm and experienced 17% higher egg-hatching success, compared with those mated to no-gift males, despite matched copulation durations. Uninterrupted copulations resulted in both increased sperm storage and egg-hatching success. Our study confirms the prediction that the nuptial gift as a male signal is under positive sexual selection by females through cryptic sperm storage. In addition, the gift facilitates longer copulations and increased sperm transfer providing two different types of advantage to gift-giving in males.     

The relative influence of prey abundance and co-breeders on the reproductive performance of polyandrous Pale Chanting-goshawks

This study investigates if the reproductive performance of polyandrous Pale Chanting-goshawks, Melierax canorus, is governed by the abundance of dominant rodent-prey species or a co-breeding male participating fully in prey being delivered to the female and young. Polyandrous trios in prey-rich habitat, the only habitat where these trios occurred, failed to produce more offspring than monogamous pairs, but attempted more second broods in years of high prey abundance. The higher the prey-delivering rates at the nesting sites by either one monogamous male or two polyandrous males (combined effort), the higher the proportion of time their females spent in close proximity to the nest. Since there were no significant differences between the body masses of nestlings fledged by polyandrous and monogamous groups, higher delivery rates relieved females from away-from-the-nest hunting duties and permitted them to feed on prey not fed to offspring. Although breeding in polyandrous trios held fitness benefits for females, e.g. to accumulate the necessary body reserves for laying a second clutch in years of high prey abundance, it is still not clear how males benefited. The reproductive performance of each group was strongly linked to the abundance of the dominant, otomyine rodent prey (Otomys unisulcatus and Parotomys brantsii) and it was therefore prey abundance, and not the number of males delivering prey to the female and nestlings at each nesting site, that controlled the reproductive performance of cooperative-breeding Pale Chanting-goshawks.