Sexual conflicts along gradients of density and predation risk: insights from an egg-trading fish

In principle, the intensity of sexual conflict is best measured as a loss of fitness associated with the expression of conflict-related traits. But because the relevant traits may be difficult to manipulate and fitness difficult to assess, proxy variables linked to conflict intensity may provide important tools for empirical measurement. Here we identify two common types of sexual conflict—one within mating pairs over the less expensive male role, and one between mating pairs and intruders seeking to obtain fertilizations—and consider how they vary in intensity along gradients of population density and predation risk. To do this, we develop and analyze a model of mating dynamics in the chalk bass, an egg-trading simultaneous hermaphrodite that lives on Caribbean coral reefs. In this species, within-pair sexual conflict leads each female-role partner to provide in each mating episode only a subset (parcel) of its egg clutch to its mate for fertilization. Pair-intruder sexual conflict (i.e., sperm competition) increases the proportion of the gonad allocated to male function. In the model, more parceling and greater male allocation both resulted in lower fitness at the ESS, our measure of conflict intensity. Male allocation increased along the density gradient but decreased along the predation-risk gradient, reflecting shifts in intrusion frequency. Parcel number sharply increased and then decreased more gradually along a gradient of increasing local density, initially responding to increased availability of alternative mates across low densities and then to diminishing clutch size toward higher densities. Parcel number decreased with predation risk as each mating episode became more dangerous. Conflict intensities were usually greatest at intermediate positions along the two environmental gradients, and each conflict ameliorated the intensity of the other. Overall, parceling and sex allocation may be good though imperfect proxies for intensities of within-pair and pair-intruder sexual conflicts among chalk bass.     

Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics

Female remating rate dictates the level of sperm competition in a population, and extensive research has focused on how sperm competition generates selection on male ejaculate allocation. Yet the way ejaculate allocation strategies in turn generate selection on female remating rates, which ultimately influence levels of sperm competition, has received much less consideration despite increasing evidence that both mating itself and ejaculate traits affect multiple components of female fitness. Here, we develop theory to examine how the effects of mating on female fertility, fecundity and mortality interact to generate selection on female remating rate. When males produce more fertile ejaculates, females are selected to mate less frequently, thus decreasing levels of sperm competition. This could in turn favour decreased male ejaculate allocation, which could subsequently lead to higher female remating. When remating simultaneously increases female fecundity and mortality, females are selected to mate more frequently, thus exacerbating sperm competition and favouring male traits that convey a competitive advantage even when harmful to female survival. While intuitive when considered separately, these predictions demonstrate the potential for complex coevolutionary dynamics between male ejaculate expenditure and female remating rate, and the correlated evolution of multiple male and female reproductive traits affecting mating, fertility and fecundity.     

SEX ALLOCATION ADJUSTMENT TO MATING GROUP SIZE IN A SIMULTANEOUS HERMAPHRODITE

Sex allocation theory is considered as a touchstone of evolutionary biology, providing some of the best supported examples for Darwinian adaptation. In particular, Hamilton's local mate competition theory has been shown to generate precise predictions for extraordinary sex ratios observed in many separate‐sexed organisms. In analogy to local mate competition, Charnov's mating group size model predicts how sex allocation in simultaneous hermaphrodites is affected by the mating group size (i.e., the number of mating partners plus one). Until now, studies have not directly explored the relationship between mating group size and sex allocation, which we here achieve in the simultaneously hermaphroditic flatworm Macrostomum lignano. Using transgenic focal worms with ubiquitous expression of green‐fluorescent protein (GFP), we assessed the number of wild‐type mating partners carrying GFP+ sperm from these focal worms when raised in different social group sizes. This allowed us to test directly how mating group size was related to the sex allocation of focal worms. We find that the proportion of male investment initially increases with increasing mating group size, but then saturates as predicted by theory. To our knowledge, this is the first direct test of the mating group size model in a simultaneously hermaphroditic animal.     

Access to multiple mates increases fecundity but does not affect per‐offspring maternal investment in a marine gastropod

Females of many organisms mate more than once and with more than one male, suggesting that polyandry confers some advantage to the female or her offspring. However, variation in maternal investment in response to mate choice and mate number can confound efforts to determine if there are benefits of polyandry. Access to multiple mates could increase maternal investment in offspring via a number of different mechanisms. Few studies have determined if investment is influenced by mate choice and number, and data are particularly lacking for marine invertebrates. This study was designed to determine if maternal investment and offspring size increase with access to increasing numbers of mates in the protandrous intertidal slipper snail Crepidula cf. marginalis. Virgin female slipper limpets were exposed to one, three, or five potential mates and their fecundity, egg size, and hatchling size were measured for multiple clutches. Treatment had a significant effect on fecundity, with fecundity increasing with the number of potential mates. Treatment did not have an effect on the size of eggs or hatchlings, on the variation in egg size or hatchling size within broods, or on the frequency of oviposition. Treatment did alter the variation in average offspring size among females, but not in the way predicted by theory. The main result, that access to multiple mates does not have an effect on per offspring maternal investment, makes C. cf. marginalis an ideal candidate to study the effects of polyandry on offspring fitness without having to take into account confounding effects of variation in maternal investment.     

SPERM COMPETITION GAMES: A GENERAL MODEL FOR PRECOPULATORY MALE–MALE COMPETITION

Reproductive males face a trade‐off between expenditure on precopulatory male–male competition—increasing the number of females that they secure as mates—and sperm competition—increasing their fertilization success with those females. Previous sperm allocation models have focused on scramble competition in which males compete by searching for mates and the number of matings rises linearly with precopulatory expenditure. However, recent studies have emphasized contest competition involving precopulatory expenditure on armaments, where winning contests may be highly dependent on marginal increases in relative armament level. Here, we develop a general model of sperm allocation that allows us to examine the effect of all forms of precopulatory competition on sperm allocation patterns. The model predicts that sperm allocation decreases if either the “mate‐competition loading,”a, or the number of males competing for each mating, M, increases. Other predictions remain unchanged from previous models: (i) expenditure per ejaculate should increase and then decrease, and (ii) total postcopulatory expenditure should increase, as the level of sperm competition increases. A negative correlation between a and M is biologically plausible, and may buffer deviations from the previous models. There is some support for our predictions from comparative analyses across dung beetle species and frog populations.     

Reproductive costs of mating with a sibling male: sperm depletion and multiple mating in Cephalonomia hyalinipennis

Polygynous parasitoid males may be limited by the amount of sperm they can transmit to females, which in turn may become sperm limited. In this study, I tested the effect of male mating history on copula duration, female fecundity, and offspring sex ratio, and the likelihood that females will have multiple mates, in the gregarious parasitoid Cephalonomia hyalinipennis Ashmead (Hymenoptera: Bethylidae: Epyrinae), a likely candidate for sperm depletion due to its local mate competition system. Males were eager to mate with the seven females presented in rapid succession. Copula duration did not differ with male mating history, but latency before a first mating was significantly longer than before consecutive matings. Male mating history had no bearing on female fecundity (number of offspring), but significantly influenced offspring sex ratio. The last female to mate with a given male produced significantly more male offspring than the first one, and eventually became sperm depleted. In contrast, the offspring sex ratio of first‐mated females was female biased, denoting a high degree of sex allocation control. Once‐mated females, whether sperm‐depleted or not, accepted a second mating after a period of oviposition. Sperm‐depleted females resumed production of fertilized eggs after a second mating. Young, recently mated females also accepted a second mating, but extended in‐copula courtship was observed. Carrying out multiple matings in this species thus seems to reduce the cost of being constrained to produce only haploid males after accepting copulation with a sperm‐depleted male. I discuss the reproductive fitness costs that females experience when mating solely with their sibling males and the reproductive fitness gain of males that persist in mating, even when almost sperm‐depleted. Behavioural observations support the hypothesis that females monitor their sperm stock. It is concluded that C. hyalinipennis is a species with a partial local mating system.     

Effects of Single Versus Multiple Mates: Monogamy Results in Increased Fecundity for the Beetle <Emphasis Type="Italic">Phoracantha semipunctata</Emphasis>

Effects of polyandry versus monogamy were assessed for the beetle Phoracantha semipunctata (Coleoptera: Cerambycidae) by comparing measures of female reproductive success, including fecundity, egg viability, time until eclosion, and clutch size. The effect of intermittent presence or absence of a male was also evaluated. Polyandry was detrimental to female reproductive success in comparison to monogamy. Fecundity, egg viability, and clutch size were lower, and time to eclosion were increased for eggs from females with multiple mates compared with monogamous females. Intermittent presence of males had no effect on female reproductive success. Possible explanations for the decreased fecundity experienced by females with multiple mates include sperm competition intensity, costs of male harassment, and exceeding the optimal mating frequency. Females may reduce costs associated with polyandry by spending less time on host logs where mating occurs.     

Determinants of mating and sperm‐transfer success in a simultaneous hermaphrodite

The number of mating partners an individual has within a population is a crucial parameter in sex allocation theory for simultaneous hermaphrodites because it is predicted to be one of the main parameters influencing sex allocation. However, little is known about the factors that determine the number of mates in simultaneous hermaphrodites. Furthermore, in order to understand the benefits obtained by resource allocation into the male function it is important to identify the factors that predict sperm‐transfer success, i.e. the number of sperm a donor manages to store in a mate. In this study we experimentally tested how social group size (i.e. the number of all potential mates within a population) and density affect the number of mates and sperm‐transfer success in the outcrossing hermaphroditic flatworm Macrostomum lignano. In addition, we assessed whether these parameters covary with morphological traits, such as body size, testis size and genital morphology. For this we used a method, which allows tracking sperm of a labelled donor in an unlabelled mate. We found considerable variation in the number of mates and sperm‐transfer success between individuals. The number of mates increased with social group size, and was higher in worms with larger testes, but there was no effect of density. Similarly, sperm‐transfer success was affected by social group size and testis size, but in addition this parameter was influenced by genital morphology. Our study demonstrates for the first time that the social context and the morphology of sperm donors are important predictors of the number of mates and sperm‐transfer success in a simultaneous hermaphrodite. Based on these findings, we hypothesize that sex allocation influences the mating behaviour and outcome of sperm competition.     

Male Mate Choice in the Guppy (Poecilia reticulata): Do Males Prefer Larger Females as Mates?

Although females are the choosier sex in most species, male mate choice is expected to occur under certain conditions. Theoretically, males should prefer larger females as mates in species where female fecundity increases with body size. However, any fecundity‐related benefits accruing to a male that has mated with a large female may be offset by an associated fitness cost of shared paternity if large females are more likely to be multiply mated than smaller females in nature. We tested the above hypothesis and assumption using the Trinidadian guppy (Poecilia reticulata) by behaviourally testing for male mate choice in the laboratory and by ascertaining (with the use of microsatellite DNA genotyping) patterns of male paternity in wild‐caught females. We observed significant positive relationships between female body length and fecundity (brood size) and between body length and level of multiple paternity in the broods of females collected in the Quaré River, Trinidad. In laboratory tests, a preference for the larger of two simultaneously‐presented virgin females was clearly expressed only when males were exposed to the full range of natural stimuli from the females, but not when they were limited to visual stimuli alone. However, as suggested by our multiple paternity data, males that choose to mate with large females may incur a larger potential cost of sperm competition and shared paternity compared with males that mate with smaller females on average. Our results thus suggest that male guppies originating from the Quaré River possess mating preferences for relatively large females, but that such preferences are expressed only when males can accurately assess the mating status of encountered females that differ in body size.     

Seasonal Variation in Mate Choice of Photinus ignitus Fireflies

Mate choice by either sex may vary with changes in the associated costs and benefits, determined by factors such as the availability of potential mates and variation in mate quality. We examined seasonal variation in operational sex ratio, courtship behavior, spermatophore mass, egg count, and the relationship between morphological traits and mating success in Photinus ignitus fireflies to determine if mate choice in either sex varied with the availability and relative reproductive investment of fertilizable females and sexually active males. Successfully mating males had larger lanterns than unsuccessful males when the operational sex ratio was male‐biased. In addition, female responsiveness to male signals increased as the number of courting males decreased, and male spermatophore mass decreased with body size across the mating season. Successfully mating females had larger body mass than unsuccessful females. Female body mass predicted egg count and female rejection by males increased as the season progressed and female size decreased. These results suggest that both male and female P. ignitus exhibit mate choice, and that such choice is influenced by seasonal variation in the abundance and quality of potential mates.     

Evolutionary stable sex ratios with non‐facultative male‐eggs first sex allocation in fig wasps

Sex allocation theory has long generated insights into the nature of natural selection. Classical models have elucidated causal phenomena such as local mate competition and inbreeding on the degree of female bias exhibited by various invertebrates. Typically, these models assume mothers facultatively adjust sex allocation using predictive cues of future offspring mating conditions. Here we relax this assumption by developing a sex allocation model for haplodiploid mothers experiencing local mate competition that lay a fixed number of male eggs first. Female egg number is determined by remaining oviposition sites or remaining eggs of the mother, depending on which is exhausted first. Our model includes parameters for variation in foundress number, patch size, fecundity and offspring mortality that allow us to generate secondary sex ratio predictions based on specific parameterizations for natural populations. Simulations show that: 1) in line with classical models, factors that increase sib‐mating result in mothers laying relatively more female eggs; 2) high offspring mortality leads to relatively more males as fertilization insurance; 3) unlike classical model predictions, sub‐optimal predictions, such as more males than females are possible. In addition, our model provides the first quantitative predictions for the expected number of males and females in a patch where typically only one mother utilizes a given patch. We parameterized the model with data obtained from seven species of southern African fig wasps to predict expected means and variances for numbers of male and female offspring for typical numbers of mothers utilizing a patch. These predictions were compared to secondary sex ratio data from single foundress patches, the most commonly encountered situation for these species. Our predictions matched both the observed number and variance of male and female offspring with a high degree of accuracy suggesting that facultative adjustment is not required to produce evolutionary stable sex ratios.     

Multiple paternity and mate competition in non-selfing,monogamous, egg-trading hermaphrodites

In animals in which the two sexes invest relatively similar amounts of resources in their young, the number of mates is expected to affect male and female reproductive success similarly and gender conflicts on the number of mates may not arise. Correspondingly, in non-selfing, simultaneous hermaphrodites with long-term monogamy, the two partners are expected to alternate repeatedly their sexual roles and invest similarly in their offspring. Therefore, the gender conflict on the number of mating partners should not arise. However, when >2 conspecifics are present, hermaphrodites are known to plastically adjust their behavior and sex allocation and compete for mating repeatedly in the male role. We tested whether this leads to multiple paternities of single egg clutches in experimental replicates of small and large groups of non-selfing, egg-trading, behaviorally monogamous polychaete worms (Ophryotrocha diadema) by using neutral genetic markers to estimate paternity. Multiply fertilized egg cocoons were common in these worms; two or more individuals succeeded in fertilizing the same egg cocoon and mate competition increased with group size. Multiply fertilized egg cocoons had a higher proportion of eggs developing into mature worms than singly fertilized egg cocoons. Possibly singly fertilized cocoons had a lower fertilization rate owing to low sperm counts and aflagellate sperm.     

Male size determines reproductive output in a paternal mouthbrooding fish

Size can have strong effects on reproductive success in both males and females, and in many species large individuals are preferred as mates. To estimate the potential benefits from mate choice for size in both sexes, I studied the effects of the size of each sex on the reproductive output of pairs of Banggai cardinalfish, Pterapogon kauderni, a sexually monomorphic obligate paternal mouthbrooder. When pairs were allowed to form freely, a size-assortative mating pattern was observed and larger pairs had a higher reproductive output as determined by total clutch weight and egg size. To separate the potential benefits from mate choice for size for each sex, I subsequently used these pairs to form reversed size-assortative pairs, that is, the largest male paired to the smallest female and vice versa. I found a positive correlation between male size and clutch size: relatively heavier clutches were found in pairs where females were given a larger male. This suggests that the size of the male influences clutch weight. For egg size, however, the size of both sexes seemed important. The study reveals the benefits of mutual mate choice on size in this species: larger females provide larger eggs and larger males can brood heavier clutches. Furthermore, these results suggest that females differentially allocate resources into the eggs according to the size of the mate.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Size-biased Mating in Both Sexes of the Black-horned Tree Cricket, <Emphasis Type="Italic">Oecanthus nigricornis</Emphasis> Walker (Orthoptera: Gryllidae: Oecanthinae)

Previous studies on tree crickets have demonstrated female choice of males based on size and courtship feeding but less is known about sexual selection under conditions of direct mating competition. I studied courtship, aggression and mating of the black-horned tree cricket Oecanthus nigricornis (Walker) to test size-related sexual selection under conditions of direct sexual competition. Results show that larger individuals of both sexes mated more frequently than their smaller counterparts, and this was due to the ability of large individuals to out compete rivals. Large males achieved the advantage by aggressively reducing courtship by small males, whereas large females responded to male courtship more quickly but with little aggression. Although there was no evidence here for mate choice, there were advantages for having larger mates; fecundity increased with female size and spermatophores (which females consume after mating) increased with male size. Size of the specialized metanotal courtship gift, however, was not related to male size.     

Size‐Dependent Male Mate Preference and its Association with Size‐Assortative Mating in a Mangrove Snail,Littoraria ardouiniana

In many animals, body size plays a crucial role in mating success in the context of competition and preference for mates. Increasing evidence has shown that male mate preference can be size‐dependent and, therefore, an important driver of size‐assortative mating. To test this theory, mate choice experiments were performed during the three consecutive stages of mating behaviour, namely trail following, shell mounting and copulation, in the dioecious mangrove snail, Littoraria ardouiniana. These experiments identified two possible forms of size‐dependent male mate preference which could contribute to the formation of size‐assortative mating in these snails. Firstly, whereas small males were unselective, large males were selective and preferred to follow mucus trails laid by large females. Alternatively, the results can also be interpreted as all males were selective and adopted a mating strategy of selecting females similar to, or larger than, their own sizes. Both small and large males also copulated for longer with large than with small females, and this was more pronounced in large males. When two males encountered a female, they engaged in physical aggression, with the larger male excluding the smaller male from copulating with the female. This study, therefore, demonstrated that size‐dependent male mate preference may, along with male–male competition, play an important role in driving size‐assortative mating in these mangrove snails, and this may also be the case in other species that exhibit male mate choice.     

Sperm competition and the significance of female multiple mating in the predatory miteParasitus fimetorum

Females of the predatory miteParasitus fimetorum (Gamasida; Parasitina) inhabiting animal manure indiscriminately copulate with many mates. The sperm competition between the males was estimated by electrophoresis of allozymes and the effects of multiple mating on female reproduction were investigated. When females were forced to mate only once, their fecundity decreased drastically compared to the case of multiple mating (but longevity was unaffected). When one female mated with two males, the outcome of sperm competition depended greatly upon the mating interval. When the second mating occurred immediately after the first, the female fecundity decreased as in the case of single mating and the second male fertilized only a few eggs. However, when there was an interval of 1 day between the two matings, the females achieved normal fecundity and the second male fertilized approximately half the eggs. This suggests that the spermatophore deposited by the first male may act as a short-term copulatory ‘plug’ in the female's genital opening. When one female mated with several males with 1 day intervals, three or more males shared fertilization of the eggs. This study suggests that the multiple mating of females is a necessary stimulus to continue oogenesis and some physiological factors for this stimulation may exist in spermatophores.     

Female and Male Moths Display Different Reproductive Behavior when Facing New versus Previous Mates

Multiple mating allows females to obtain material (more sperm and nutrient) and/or genetic benefits. The genetic benefit models require sperm from different males to fertilize eggs competitively or the offspring be fathered by multiple males. To maximize genetic benefits from multiple mating, females have evolved strategies to prefer novel versus previous mates in their subsequent matings. However, the reproductive behavior during mate encounter, mate choice and egg laying in relation to discrimination and preference between sexes has been largely neglected. In the present study, we used novel and previous mate treatments and studied male and female behavior and reproductive output in Spodoptera litura. The results of this study do not support the sperm and nutrient replenishment hypotheses because neither the number of mates nor the number of copulations achieved by females significantly increased female fecundity, fertility and longevity. However, females showed different oviposition patterns when facing new versus previous mates by slowing down oviposition, which allows the last male has opportunities to fertilize her eggs and the female to promote offspring diversity. Moreover, females that have novel males present called earlier and more than females that have their previous mates present, whereas no significant differences were found on male courtship between treatments. These results suggest that S. litura females can distinguish novel from previous mates and prefer the former, whereas males generally remate regardless of whether the female is a previous mate or not. In S. litura, eggs are laid in large clusters and offspring competition, inbreeding and disease transfer risks are thus increased. Therefore, offspring diversity should be valuable for S. litura, and genetic benefits should be the main force behind the evolution of female behavioral strategies found in the present study.     

Pairing and insemination patterns in a giant weta (Deinacrida rugosa: Orthoptera; Anostostomatidae)

Positive size assortative mating can arise if either one or both sexes prefer bigger mates or if the success of larger males in contests for larger females leaves smaller males to mate with smaller females. Moreover, body size could not only influence pairing patterns before copulation but also the covariance between female size and size of ejaculate (number of spermatophores) transferred to a mate. In this field study, we examine the pre-copulatory mate choice, as well as insemination, patterns in the Cook Strait giant weta (Deinacrida rugosa). D. rugosa is a large orthopteran insect that exhibits strong female-biased sexual dimorphism, with females being nearly twice as heavy as males. Contrary to the general expectation of male preference for large females in insects with female-biased size dimorphism, we found only weak support for positive size assortative mating based on size (tibia length). Interestingly, although there was no correlation between male body size and the number of spermatophores transferred, we did find that males pass more spermatophores to lighter females. This pattern of sperm transfer does not appear to be a consequence of those males that mate heavier females being sperm depleted. Instead, males may provide lighter females with more spermatophores perhaps because these females pose less of a sperm competition risk to mates.     

Harm to females increases with male body size in Drosophila melanogaster

Previous studies indicate that female Drosophila melanogaster are harmed by their mates through copulation. Here, we demonstrate that the harm that males inflict upon females increases with male size. Specifically, both the lifespan and egg-production rate of females decreased significantly as an increasing function of the body size of their mates. Consequently, females mating with larger males had lower lifetime fitness. The detrimental effect of male size on female longevity was not mediated by male effects on female fecundity, egg-production rate or female-remating behaviour. Similarly, the influence of male size on female lifetime fecundity was independent of the male-size effect on female longevity. There was no relationship between female size and female resistance to male harm. Thus, although increasing male body size is known to enhance male mating success, it has a detrimental effect on the direct fitness of their mates. Our results indicate that this harm is a pleiotropic effect of some other selected function and not an adaptation. To the extent that females prefer to mate with larger males, this choice is harmful, a pattern that is consistent with the theory of sexually antagonistic coevolution.     

Mate Choice and Spawning Success in the Fighting Fish Betta splendens: the Importance of Body Size, Display Behavior and Nest Size

Courtship displays should be exaggerated enough to attract mates and yet tempered so as not to deter them. We tested this hypothesis in the fighting fish Betta splendens by studying courtship displays and body size and their relationships with male parental quality and female fecundity, as well as the effects of display behavior and body size on mate choice decisions and spawning success. Because of their high degree of parental investment, males are expected to be discriminating in their choice of mates. Males who displayed more frequently built larger nests, a measure of parental quality, but larger males did not. When females were paired with males with high display rates, however, the pair had fewer eggs in their nest, even when accounting for female body mass. In a mate choice test using computer‐generated male stimuli that differed only in display behavior, females showed no preferences for displaying males vs. non‐displaying males, or for males with higher display rates vs. lower display rates. In similar tests in which the computer‐generated males differed only in size, females preferred larger males, but also preferred males that differed with respect to body size (negative assortative mating). Males preferred computer‐generated females that performed courtship displays over non‐displaying females, but showed no preferences for female body size. Neither a female's body size nor her display behavior was a significant predictor of her fecundity as estimated by the number of eggs released during spawning. Thus, our results suggest that female B. splendens must balance male parental quality (nest size) with the risk of potentially disruptive or dangerous behavior during spawning, and that females may minimize these risks through negative size‐assortative mating. Female display behavior, while unrelated to fecundity in our study, may attract males because it indicates reproductive readiness or serves a species‐recognition function.