Prior oviposition, female receptivity and last-male sperm precedence in the cosmopolitan pest Callosobruchus maculatus (Coleoptera: Bruchidae)

Sperm competition studies have shown that P₂ (the proportion of ova fertilized by the last male to mate) increases as the interval between inseminations is experimentally increased. Variation in the number of sperm in storage is associated with sperm use (or loss) from the female's sperm stores between copulations (fewer sperm from previous mates at the time of the last copulation) and with the extent of prior oviposition and female receptivity to further copulation: females that lay many eggs tend to have few remaining sperm in storage and to be more receptive to further copulation. Using the bruchid beetle Callosobruchus maculatus, we examined the effect of prior oviposition and female receptivity to further copulation on the extent of last-male sperm precedence (measured as P₂). Extent of prior oviposition was experimentally manipulated independently of the intermating interval by altering the availability of oviposition sites between inseminations. Females given few or no oviposition sites laid fewer eggs, were less receptive and had a lower P₂ than females given abundant oviposition sites. To examine the effect of female receptivity on P₂ independently of prior oviposition, we examined the outcome of sperm competition experiments using (1) females from lines that had been selected for different latencies to copulation and (2) natural variation in female latency to receptivity. Female receptivity to further copulation had no detectable effect on P₂. When oviposition resource is abundant, female receptivity may be a poor predictor of current sperm load.     

High multiple paternity and low last-male sperm precedence in a hermaphroditic planarian flatworm: consequences for reciprocity patterns

It is difficult to predict a priori how mating success translates into fertilization success in simultaneous hermaphrodites with internal fertilization. Whereas insemination decisions will be determined by male interests, fertilization will depend on female interests, possibly leading to discrepancies between insemination and fertilization patterns. The planarian flatworm Schmidtea polychroa, a simultaneous hermaphrodite in which mating partners trade sperm was studied. Sperm can be stored for months yet individuals mate frequently. Using microsatellites, maternity and paternity data were obtained from 748 offspring produced in six groups of 10 individuals during four weeks. Adults produced young from four mates on average. Reciprocal fertilization between two mates was found in only 41 out of 110 registered mate combinations, which is clearly less than what is predicted from insemination patterns. Multiple paternity was high: > 80% of all cocoons had two to five fathers for only three to five offspring per cocoon. Because animals were collected from a natural population, 28% of all hatchlings were sired by unknown sperm donors in the field, despite a 10-day period of acclimatization and within-group mating. This percentage decreased only moderately throughout the experiment, showing that sperm can be stored and used for at least a month, despite frequent mating and sperm digestion. The immediate paternity a sperm donor could expect to obtain was only about 25%. Male reproductive success increased linearly with the number of female partners, providing support for Bateman's principle in hermaphrodites. Our results suggest that hermaphrodites do not trade fertilizations when trading sperm during insemination, lending support to the view that such conditional sperm exchange is driven by exchange of resources.     

Sperm competition and sperm precedence in the dragonfly Nanophya pygmaea

Abstract. The libellulid dragonfly, Nanophya pygmaea Rambur, has an average ejaculate volume of 0.16 mm³. During successive copulations the volume of sperm stored in the female's sperm storage organs increases in steps equivalent to this volume, suggesting that the sperm competition mechanism in this species is sperm repositioning, i.e. adding an ejaculate to what is already present in the female's sperm storage organ. By using sterile/normal males in double matings with females we have shown that this mechanism results in last male sperm precedence (P²= 0.979).     

Number of mating males and mating interval affect last-male sperm precedence in Tenebrio molitor L.

Polyandrous females often mate with more than two males, and yet most studies of postcopulatory sexual selection involve only two males. In insects, second-male sperm precedence is usually taken as evidence of overall last-male sperm precedence despite some studies to the contrary. Furthermore, the processes or mechanisms causing the patterns are often unknown and yet are important when estimating how postcopulatory sexual selection might act on males. Whether the patterns and processes change in normal sperm competitive situations and the effects of other factors besides mating order need to be examined to better assess the evolutionary potential of postcopulatory sexual selection. In this study, I assessed the effects of mating interval and number of mating males on sperm precedence patterns and their causal mechanisms in the mealworm beetle, Tenebrio molitor. Last-male sperm precedence was the same when two or three males mated, but also depended on mating intervals and hence mechanisms of paternity bias. However, when females mated with many males, one of the mechanisms no longer created last-male sperm precedence. This example illustrates the importance of knowing both the patterns and mechanisms of paternity bias and whether they change depending on female mating frequency to make reasonable inferences about the potential for postcopulatory sexual selection on males. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Chromosomal effects on male and female components of sperm precedence in Drosophila

Recent experiments with Drosophila have demonstrated that the success of sperm in multiply mated females depends on the genotype of both the male and the female. To further characterize the distinction between male and female roles in sperm success, we scored variation in both sexes in sperm competitive ability among a set of chromosome replacement lines that allow identification of effects to each chromosome. We detected significant male and female effects on sperm precedence, defined as the ability of a male's ejaculate to displace resident sperm (P2) or avoid being displaced by subsequent matings (P1). Tests of effects of first, second and third chromosome substitutions revealed significant differences among third chromosomes in male sperm precedence (both P1 and P2) and a first x second chromosome interaction in female's effect on sperm precedence (only P1). We found no significant correlation between male and female effects on sperm precedence, suggesting that the variation found in both P1 and P2 has a different genetic cause in the two sexes.     

Female choice, male interference, and sperm precedence in the red-spotted newt

Darwin first identified female choice and male—male competitionas forms of sexual selection resulting in the evolution of conspicuoussexual dimorphism, but it has proven challenging to separatetheir effects. Their effects on sexual selection become evenmore complicated when sperm competition occurs because spermprecedence may be either a form of cryptic female choice ora form of male—male competition. We examined the effectsof tail height on male—male competition and female choiceusing the sexually dimorphic red-spotted newt (Notophthalmusviridescens viridescens). Experiment 1 examined whether maletail height influenced male mating success. Males with deeptails were more successful at mating with females than thosewith shallow tails. Successful, deep-tailed males also were bigger(snout-vent length; SVL) than unsuccessful, shallow-tailed males,but they did not vary in tail length or body condition. Of these,only tail height and tail length are sexually dimorphic traits.Experiment 2 tested the hypothesis that the differential successof males with deeper tails was due to female choice by examiningboth simultaneous female preference for association and sequentialfemale choice. We found no evidence of female choice. When maleswere not competing to mate with females, tail height did notinfluence male mating success. Successful males did not havedifferent SVL and tail lengths than unsuccessful males. Thus,tail height in male red-spotted newts appears to be an intrasexuallyselected secondary sexual characteristic. Experiment 3 usedpaternity exclusion analyses based on molecular genetic markersto examine the effect of sperm precedence on sperm competitionin doubly-mated females. Sperm precedence likely does not havea pervasive and consistent effect on fertilization success becausewe found evidence of first, last, and mixed sperm usage.     

Female genotype affects male success in sperm competition

The central question addressed by most studies of sperm competition is: ''what determines which male''s sperm are used at fertilization?'' Empirical and theoretical studies that address this question have traditionally focused on adaptations which enhance male fertilization success while treating the female as a receptacle in which sperm competition is played out. Here we provide evidence which suggests that female genotype strongly influences the outcome of sperm competition. When the sperm of two males are in competition the proportion of offspring fathered by the second male to mate (P₂) was found to be highly repeatable only if the male pair were mated to three different, but genetically similar females (full-sisters to each other; unrelated to either of the males). In contrast, if a male pair were mated to three females that were unrelated then P₂ was either non-repeatable or marginally repeatable. We also show that male success in sperm competition is determined, to a large extent, by gamete and/or male–female compatibility. This conclusion is derived from the observation that P₂ was repeatable among full-sisters mated to different, yet genetically similar male pairings, whilst P₂ was non-repeatable among full-sisters mated to different, genetically distinct male pairings.     

Female remating and sperm competition patterns in a terrestrial crustacean

In most species, both sexes may mate with more than one partner during their life. In terrestrial isopods (woodlice) female remating can occur within a reproductive season (immediate remating) or after a period of sexual rest and sperm storage, that is in a subsequent reproductive season (delayed remating). The pattern of sperm precedence is unknown in both cases. These two female remating patterns may shape male-male competition in different ways. To elucidate both patterns of female remating and sperm precedence, we used an albinism mutation in Armadillidium vulgare to track paternity in laboratory experiments. Males had low remating success after immediate remating attempts, mainly because of the female's refractory behaviour. However, refractory behaviour seemed to be lost after female sexual rest: delayed remating attempts were as successful as first mating attempts with virgin females. In both immediate and delayed remating, competing males had similar fertilization success, but varied in sperm precedence. We hypothesize that males might induce the refractory mating behaviour in females to ensure their paternity. This could be a strategy that evolved in woodlice after the loss of precopulatory mate guarding during adaptation to the terrestrial environment. We discuss the consequences of these findings for woodlice optimal mating strategies. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Female remating, sperm competition and sexual selection in Drosophila

Female remating is fundamental to evolutionary biology as it determines the pattern of sexual selection and sexual conflict. Remating in females is an important component of Drosophila mating systems because it affects sperm usage patterns and sexual selection. Remating is common in females of many species of Drosophila in both natural and laboratory populations. It has been reported in many insect species and also in vertebrates. Female remating is a prerequisite for sperm competition between males, and the consequences of this competition, such as sperm precedence or sperm displacement, have been reported for many species of Drosophila. Female remating is dependent on the amount of sperm stored, the male seminal fluid components, nutrition, the quantity of eggs laid, experimental design and density of flies in laboratory. Remating by a female is an insurance against male sterility and sub-fertility and increases genetic heterogeneity of female offspring. Remating gives greater female productivity in many species of Drosophila. We examined female remating with respect to sperm competition and sexual selection in Drosophila and addressed the possible benefits for females. We also reviewed the role of accessory gland fluid in remating, costs associated with remating, the genetic basis of female remating and some possible mechanisms of sperm competition in the light of last male sperm priority and paternity assurance in Drosophila and other insects. We also suggest future areas of research.     

Social life histories: jackdaw dominance increases with age,terminally declines and shortens lifespan

Behaviour may contribute to changes in fitness prospects with age, for example through effects of age-dependent social dominance on resource access. Older individuals often have higher dominance rank, which may reflect a longer lifespan of dominants and/or an increase in social dominance with age. In the latter case, increasing dominance could mitigate physiological senescence. We studied the social careers of free-living jackdaws over a 12 year period, and found that: (i) larger males attained higher ranks, (ii) social rank increased with age within individuals, and (iii) high-ranked individuals had shorter lifespan suggesting that maintaining or achieving high rank and associated benefits comes at a cost. Lastly, (iv) social rank declined substantially in the last year an individual was observed in the colony, and through its effect on resource access this may accelerate senescence. We suggest that behaviour affecting the ability to secure resources is integral to the senescence process via resource effects on somatic state, where behaviour may include not only social dominance, but also learning, memory, perception and (sexual) signalling. Studying behavioural effects on senescence via somatic state may be most effective in the wild, where there is competition for resources, which is usually avoided in laboratory conditions.     

Experience pays: offspring survival increases with female age

Life-history theory predicts that, in long-lived organisms, effort towards reproduction will increase with age, and research from oviparous vertebrates largely supports this prediction. In reptiles, where parental care occurs primarily via provisioning of the egg, older females tend to produce larger eggs, which in turn produce larger hatchlings that have increased survival. We conducted an experimental release study and report that maternal age positively influences offspring survivorship in the painted turtle (Chrysemys picta) and predicts offspring survival at least as well as hatchling body size does. These data suggest that, although increasing hatchling size is a major component of reproductive success in older individuals, other factors also contribute.     

Female remating in butterflies: interaction between female genotype and nonfertile sperm

Female mating rate is fundamental to evolutionary biology as it determines the pattern of sexual selection and sexual conflict. Despite its importance, the genetic basis for female remating rate is largely unknown and has only been demonstrated in one species. In paternally investing species there is often a conflict between the sexes over female mating rate, as females remate to obtain male nutrient donations and males try to prevent female remating to ensure high fertilization success. Butterflies produce two types of sperm: fertilizing, eupyrene sperm, and large numbers of nonfertile, apyrene sperm. The function of apyrene sperm in the polyandrous, paternally investing green‐veined white butterfly, Pieris napi, is to fill the female’s sperm storage organ thereby reducing her receptivity. However, there is large variation in number of apyrene sperm stored. Here, I examine the genetic basis to this variation, and if variation in number of apyrene sperm stored is related to females’ remating rate. The number of apyrene sperm stored at the time of remating has a genetic component and is correlated with female remating tendency, whereas no such relationship is found for fertilizing sperm. The duration of the nonreceptivity period in P. napi also has a genetic component and is inversely related to the degree of polyandry. Sexual conflict over female remating rate appears to be present in this species, with males using their apyrene sperm to exploit a female system designed to monitor sperm in storage. Ejaculates with a high proportion of nonfertile sperm may have evolved to induce females to store more of these sperm, thereby reducing remating. As a counter‐adaptation, females have evolved a better detection system to regain control over their remating rate. Sexually antagonistic co‐evolution of apyrene sperm number and female sperm storage may be responsible for ejaculates with predominantly nonfertile sperm in this butterfly.     

The role of sperm numbers in sperm competition and female remating in Drosophila melanogaster

Single mating productivities (used as estimates of the relative number of sperm transferred) are highly correlated with several parameters used to quantify sperm competition in D. melanogster. Matings that result in the transferal of large numbers of sperm are associated with longer delay of female remating than are matings that transfer fewer sperm. Males that transfer larger numbers of sperm also suffer a smaller proportional reduction in reproductive success (smaller COST) than males transferring fewer sperm. The number of sperm transferred by a female's second mate is not related to the COST to the first male. However, there is a high positive correlation between the number of sperm transferred by the second male and P₂ (the proportion of second male progeny following female remating). Thus, large sperm numbers apparently increase the reproductive success of males whether they mate with virgin or non-virgin females. Because female receptivity mediates these events, there is no need to invoke sperm displacement to explain the reproductive outcome of female remating.The timing of female remating is evaluated in terms of a receptivity-threshold model. This model suggests that female receptivity returns when some small, relatively constant, number of sperm remain in storage.     

Determinants of sperm precedence in a noctuid moth Heliothis virescens: a role for male age

1. Females of the noctuid moth Heliothis virescens F. mate more than once. Thus, sperm from two or more males normally compete for fertilisations within the female reproductive tract. The eggs are typically fertilised by sperm from only one male, either the female's last mate or an earlier mate. Twice‐mated females store only one ejaculate's worth of fertilising sperm (eupyrene) but nearly two ejaculates' worth of a nonfertilising sperm morph (apyrene), which is thought to play a role in sperm competition. 2. The mechanism of sperm use in H. virescens was investigated by examining factors that vary with paternity, which was assigned based on allozyme variation. The factors included male and female body masses and ages, male genital characters, the size of the sperm package, and the number of sperm stored by the female. 3. One male typically gained sperm precedence; this was nearly twice as likely to be the second male as it was to be the first. Two factors were found to vary significantly with paternity: female mass and male age. The second male to mate was more likely to gain sperm precedence if the female was larger and if the male was older than the female's first mate. 4. The significance of male age and female mass to several hypothetical models of the mechanism of sperm use is discussed.     

Influence of female age, sperm senescence and multiple mating on sperm viability in female Drosophila melanogaster

Sperm viability has been associated with the degree of promiscuity across species, as well as the degree of reproductive success within species. Thus, sperm survival within the female reproductive tract likely plays a key role in how mating systems evolve. In the fruit fly, Drosophila melanogaster, however, the extent and cause of sperm death has been the subject of recent debate. Here, we assess sperm death within the female reproductive tract of D. melanogaster following single and multiple matings in order to elucidate the extent of death and its potential mechanisms, including an acute female response to mating, female age and/or sperm senescence. We found no evidence that sperm viability was influenced by an acute female response or female age. We also found that rival ejaculates did not influence viability, supporting recent work in the system. Instead, the majority of death appears to be due to the aging of male gametes within the female, and that at least some dead resident sperm remain in the female after multiple mating. In contrast to earlier in vivo work, we found that overall sperm death was minimal (8.7%), indicating viability should have a negligible influence on female remating rates.     

Semen displacement as a sperm competition strategy

Using a sample of 652 college students, we examined several implications of the hypothesis that the shape of the human penis evolved to enable males to substitute their semen for those of their rivals. The incidence of double mating by females appears sufficient to make semen displacement adaptive (e.g., one in four females acknowledge infidelity, one in eight admit having sex with two or more males in a 24-hour period, and one in 12 report involvement in one or more sexual threesomes with two males). We also document several changes in post-ejaculatory behavior (e.g., reduced thrusting, penis withdrawal, loss of an erection) which may have evolved to minimize displacement of the male’s own semen. Consistent with predictions derived from a theoretical model (Gallup and Burch 2006), we discovered that most females report waiting at least 48 hours following an instance of infidelity before resuming sex with their in-pair partners.     

Gamete evolution and sperm numbers: sperm competition versus sperm limitation

Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization (N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization (F) and increasing sperm numbers (x) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups.     

A two-second delay confers first-male fertilization precedence within in vitro sperm competition experiments in Atlantic salmon

In vitro paired-male sperm competition experiments in Atlantic salmon Salmo salar for a single female's eggs revealed that 2 s delays in sperm release caused significant reductions in paternity, with second males achieving only 30% fertilization success (against an expected 50%). This first-male fertilization precedence supports previous work suggesting that sperm competition follows the principles of a race in Atlantic salmon, and suggests that any timing asymmetry in sperm release within natural competitive spawnings could have significant consequences for male fertilization success.     

Nest predation,food, and female age explain seasonal declines in clutch size

The selection pressures responsible for intra- and interspecific variation in avian clutch size have been debated for over half a century. Seasonal declines in clutch size represent one of the most robust patterns in avian systems, yet despite extensive research on the subject, the mechanisms underlying this pattern remain largely unknown. We tested a combination of experimental and observational predictions to evaluate ten hypotheses, representing both evolutionary and proximate mechanisms proposed to explain seasonal declines in avian clutch size. In line with long held life-history theory, we found strong support for both an evolved and proximate response to food availability for young. We also found evidence consistent with predictions that proximate level experiential nest predation influences seasonal declines in clutch size. Finally, older females appear to invest more in reproduction (initiate nests earlier and lay larger clutches) and choose better territories than younger females. Our results highlight the importance of examining multiple hypotheses in a theoretical context to elucidate the ecological processes underlying commonly observed patterns in life history.