Sperm competition games: sperm selection by females

We analyse a co-evolutionary sexual conflict game, in which males compete for fertilizations (sperm competition) and females operate sperm selection against unfavourable ejaculates (cryptic female choice). For simplicity, each female mates with two males per reproductive event, and the competing ejaculates are of two types, favourable (having high viability or success) or unfavourable (where progeny are less successful). Over evolutionary time, females can increase their level of sperm selection (measured as the proportion of unfavourable sperm eliminated) by paying a fecundity cost. Males can regulate sperm allocations depending on whether they will be favoured or disfavoured, but increasing sperm allocation reduces their mating rate. The resolution of this game depends on whether males are equal, or unequal. Males could be equal: each is favoured with probability, p, reflecting the proportion of females in the population that favour his ejaculate (the 'random-roles' model); different males are favoured by different sets of females. Alternatively, males could be unequal: given males are perceived consistently by all females as two distinct types, favoured and disfavoured, where p is now the frequency of the favoured male type in the population (the 'constant-types' model). In both cases, the evolutionarily stable strategy (ESS) is for females initially to increase sperm selection from zero as the viability of offspring from unfavourable ejaculates falls below that of favourable ejaculates. But in the random-roles model, sperm selection decreases again towards zero as the unfavourable ejaculates become disastrous (i.e. as their progeny viability decreases towards zero). This occurs because males avoid expenditure in unfavourable matings, to conserve sperm for matings in the favoured role where their offspring have high viability, thus allowing females to relax sperm selection. If sperm selection is costly to females, ESS sperm selection is high across a region of intermediate viabilities. If it is uncostly, there is no ESS in this region unless sperm limitation (i.e. some eggs fail to be fertilized because sperm numbers are too low) is included into the model. In the constant-types model, no relaxation of sperm selection occurs at very low viabilities of disfavoured male progeny. If sperm selection is sufficiently costly, ESS sperm selection increases as progeny viability decreases down towards zero; but if it is uncostly, there is no ESS at the lowest viabilities, and unlike the random-roles model, this cannot be stabilized by including sperm limitation. Sperm allocations in the ESS regions differ between the two models. With random roles, males always allocate more sperm in the favoured role. With constant types, the male type that is favoured allocates less sperm than the disfavoured type. These results suggests that empiricists studying cryptic female choice and sperm allocation patterns need to determine whether sperm selection is applied differently, or consistently, on given males by different females in the same population.     

Sperm storage by females of the polyandrous noctuid moth Heliothis virescens

Female tobacco budworm moths, Heliothis virescens, generally mate with more than one male, receiving from each mate both fertilizing sperm (eupyrene) and nonfertilizing anucleate sperm (apyrene), which is thought to play a role in sperm competition. One male typically gains sperm precedence, but it is not consistently the last or the first male to mate. I investigated the mechanism of this variable pattern of paternity by examining the patterns of storage of both types of sperm in the female's spermatheca as a function of multiple mating and male phenotype. The number of stored apyrene sperm varied with mating history, being greatest in twice-mated females and least in females mated to one nonvirgin male. In contrast, only one ejaculate's worth of eupyrene sperm was stored regardless of female mating history (once or twice mated). Thus, while they store two complements of apyrene sperm, twice-mated females apparently store only one ejaculate's worth of eupyrene sperm. This biased pattern of sperm storage may contribute to the variable pattern of paternity observed in this species. Eupyrene sperm storage also correlated positively with female size, male age and spermatophore size. Finally, a new sperm storage site was identified and described. It is a bulged region in the seminal duct. Copyright 2000 The Association for the Study of Animal Behaviour.     

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.     

Sperm release and use at fertilization by yellow dung fly females (Scathophaga stercoraria)

Females of many species mate multiple times and store transferred sperm in storage organs. The mechanisms underlying sperm release from the stores at fertilization remain poorly understood, although they are central to an understanding of the female influence on post-copulatory male competition. Using double-mated females of the yellow dung fly, we counted the sperm sticking to the surface of deposited eggs of two successive clutches to obtain insight into the physiological processes associated with fertilization. The number of sperm released to fertilize an egg decreased between the first and second clutches, as well as within clutches from early to late eggs. These results indicate that: (1) sperm are lost from the stores over time independent of egg laying and (2) the number of sperm released depends on the amount of sperm stored. The lower number of sperm on eggs of the second clutches was accompanied by a strong increase of the proportion of sperm adhering to the micropyle region, suggesting that sperm use is more efficient and sperm release better controlled when sperm supply is substantially reduced. Finally, our approach indicates that sperm storage capacity of the female is higher than assumed from counts of spermathecal sperm.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 511–518.     

Sequential mate choice by multiply mating smooth newts: females become more choosy

In some species, females sequentially mate with different maleswithin a single mating period, store sperm until the eggs areeventually fertilized, and gain no other resources from themales. Halliday hypothesized that, for such species, a femalecould ensure fertilization of her eggs by mating with the firstmale that she encounters; thereafter, she can maximize the qualityof her progeny by sampling further males and by mating onlywith males of higher quality than previously mated males. Thishypothesis predicts that females' choosiness will increase asthe breeding season progresses. We tested this prediction ofHalliday's hypothesis by examining mate choice by female smoothnewts (Triturus vulgaris vulgaris). Males of this species developa dorsal crest during the courtship season. Crest height variesbetween males and is potentially an indicator of male quality.Initially, female smooth newts were equally willing to matewith males with low or high crests. However, in their secondmating, females remated only with high-crested males. Theseresults support our prediction and are consistent with Halliday'shypothesis. If crest height in smooth newts is an indicatorof quality, this change in females' mate choice criterion allowsfemales both to initiate egg-laying very early in the seasonand, subsequently, to mate preferentially with higher qualitymates     

Mating status affects female choice when females are signalers

Sexual selection in animals has been mostly studied in species in which males are signalers and females are choosers. However, in many species, females are (also) signalers. In species with non‐signaling females, virgin females are hypothesized to be less choosy than mated females, as virgins must mate to realize fitness and the number of available males is generally limited. Yet, when females signal to attract males, mate limitation can be overcome. We tested how virgin and mated females differ in their calling behavior, mating latency, and in mate choice, using the tobacco budworm Chloridea (Heliothis) virescens as an example for a species in which females are not only choosers but also signalers. We found that virgin females signaled longer than mated females, but virgin and mated signaling females were equally ready to mate, in contrast to non‐signaling females. However, we found that virgin signaling females showed weaker mate preference than mated females, which can be explained by the fact that females increase their fitness with multiple matings. Mated females may thus further increase their fitness by more stringent mate selection. We conclude that signaling is a crucial aspect to consider when studying female mate choice because signaling may affect the number of available mates to choose from.     

Mate‐choice copying by females: the advantages of a prudent strategy

Mate choice by females may be influenced by both advertizing traits of males, and behaviour of other females. Here, a simple genetic and behavioural model studies the advantages of mate‐choice copying. From a genetic point of view, a female preferring to copy others’ mate choice adopts a prudent strategy, because her offspring will inherit the same alleles from their father as the other young in the population. The model predicts that a female should copy others’ mate‐choice, unless she encounters a relatively more attractive male than the one she has observed mating, and the attractiveness of the male reflects his genotype. For low or moderate reliability of male signalling, mate‐copying is always predicted, even if the newcoming male is more attractive than the first male. This effect is attenuated, however, when the number of females that have already chosen the first male increases.     

Sperm storage and arrangement within females of the arctiid moth Utetheisa ornatrix

Female Utetheisa ornatrix mate prolifically, a behavior that accrues nuptially transferred gifts of nutrient and defensive alkaloids from males. This behavior also potentially places sperm from numerous males in competition within the female reproductive tract. Here, we investigate sperm interactions within female U. ornatrix by exploring the arrangement and numbers of sperm stored within the spermatheca and by examining sperm deposition in the pseudobursa, a presumed digestive organ in the female reproductive tract. Our results show that females store fewer sperm than they receive from their numerous mates, and the data suggest that unwanted sperm is either shunted to the pseudobursa or expelled from the spermatheca. We found no evidence that the apyrene, or non-nucleated, sperm morph common to the Lepidoptera are involved in forming barriers between ejaculates within the spermatheca. Female U. ornatrix are thus able to control sperm use, which we argue may contribute to the pattern of paternity observed in this species.     

Strategic choice handicaps when females seek high male net viability

We examine a strategic-choice handicap model in which males send costly signals to advertise their quality to females. Females are concerned with the net viability of the male with whom they mate, where net viability is a function of the male's quality and signal. We identify circumstances in which a signaling equilibrium would require high-quality males to send signals so much larger than those of lower-quality males (to deter mimicry by the latter) as to yield lower net viabilities for the former. This causes females to shun males who send large signals, ensuring that there is no signaling equilibrium.     

Mate choice by wild and mass‐reared females of the Mediterranean fruit fly

The sterile insect technique (SIT) is used to control Mediterranean fruit fly, Ceratitis capitata (Wiedemann), but its effectiveness is limited by low sexual competitiveness of mass‐reared males. This study investigated whether wild and mass‐reared [from a temperature sensitive lethal (tsl) genetic sexing strain] females display similar mate preferences and thus exert similar selective forces on the evolution of male courtship behaviour. Wild females preferred wild males over tsl males, whereas tsl females mated indiscriminately. The probability that mounting resulted in copulation was related to the duration of pre‐mount courtship for wild females, and wild males performed longer courtships than tsl males. Copulation occurred independently of courtship duration in tsl females. Counter to the aim of the SIT, female choice by tsl females appears to promote the evolution of male behaviour disfavoured by wild females.     

Mate choice by females of the swallowHirundo rustica: Is it repeatable?

Summary If female choice is an important component of sexual selection in a particular species, we should expect considerable inter-female differences in mate choices, and, consequently, significant repeatability of ornamental traits of subsequently chosen partners. This paper examines whether or not a female's choice of mate tail lengths and, for comparison, her choice of mate wing lengths, is repeatable between breeding seasons in a field population of the swallow,Hirundo rustica. The estimated values of repeatability were not significantly different from zero in either case, 0.152 ±0.231 (SE) and 0.241 ±0.184, respectively. Possible explanations for this observation are discussed.

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Zusammenfassung Wenn die Wahl durch das Weibchen eine wichtige Rolle in der sexuellen Selektion einer Art spielt, sollte man deutliche Unterschiede in der Partnerwahl feststellen können und folglich auch signifikante Wiederholbarkeit im Aussehen (z. B. in den Unterschieden der Ausmaße für die Paarbildung wichtiger Signalstrukturen) der von einem Weibchen in Folge ausgewählten Partner. Hier wird untersucht, ob bei der Rauchschwalbe die von einem Weibchen in aufeinanderfolgenden Brutperioden gewählten Männchen hinsichtlich Schwanz und Flügellänge signifikante Wiederholbarkeiten zeigen. Die erhaltenen Werte weichen aber für beide Merkmale nicht signifikant von Null ab. Eine Reihe möglicher Erklärungen, insbesondere aber auch die Problematik von Feldstudien zu derartigen Fragen wird diskutiert.

     

Male mate choice by the lizard Anolis carolinensis: a preference for novel females

Laboratory and field manipulations tested whether male Anolis carolinensis lizards and discriminate preference for novel females over resident females. In 16 laboratory trials, we videotaped social interactions between paired males and females during baseline session (male and resident female housed together 1-3 weeks), resident-female session (male and reintroduced resident female), and novel-female session (male and novel female with resident female removed). We examined 22 behavioural variables. Male behaviours did not differ significantly between baseline and resident-female sessions, nor did female behaviours differ significantly between baseline, resident-female and novel-female sessions. However, between resident-female and novel-female sessions, males significantly increased display rate (320%), volleys of repetitive displaying (300%) and volley length (150%), and significantly decreased the distance (375%) and number (430%) of movements travelled away from the female. We concluded that males discriminate novel females from resident females independently of female behavioural or chemical cues. In each of 18 field trials, we first videotaped baseline social interactions of the resident male and females in a naturally occurring, polygynous, breeding group. The next day, we released two novel females into the territory (so at least one female remained) and videotaped subsequent social interactions. In comparison to baseline observations, males significantly increased the proportion of time spent in female-directed activities (from 5% towards resident females to 53% towards the novel female) and the proportion of displays directed towards novel females (from 6% towards resident females to 51% towards the novel female), and significantly decreased the proportion of time spent in territorial activities (from 75% to 19%) and the proportion of displays used in territorial activities (from 94% to 44%). Data from both experiments indicate that males appear to distinguish among individual females, and use this ability to increase reproductive success by identifying and preferentially pursuing novel females over previously inseminated resident females. From the perspective of cognitive ethology, we suggest a model by which males control mating decisions within their territories. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full‐sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male‐controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.     

Multiple mating and sequential mate choice in guppies: females trade up

The trade-up hypothesis outlines a behavioural strategy that females could use to maximize the genetic benefits to their offspring. The hypothesis proposes that females should be more willing to accept a mate when the new male encountered is a superior genetic source to previous mates. We provide a direct test of the trade-up hypothesis using guppies (Poecilia reticulata), and evaluate both behavioural and paternity data. Virgin female guppies were presented sequentially with two males of varying attractiveness, and their responsiveness to each male was quantified. Male attractiveness (ornamentation) was scored as the amount of orange coloration on their body. Females were generally less responsive to second-encountered males, yet responsiveness to second males was an increasing function of male ornamentation. These attractive second males also sired a greater proportion of the offspring. There was an overall tendency for last-male advantage in paternity, and this advantage was most exaggerated when the second male was more ornamented than the first. Finally, we found that our estimate of relative sperm number did not account for any significant variation in paternity. Our results suggest that female guppies may use pre-copulatory mechanisms to maximize the genetic quality of their offspring.     

Sperm competition games: the risk model can generate higher sperm allocation to virgin females

We examine the risk model in sperm competition games for cases where female fertility increases significantly with sperm numbers (sperm limitation). Without sperm competition, sperm allocation increases with sperm limitation. We define 'average risk' as the probability q that females in the population mate twice, and 'perceived risk' as the information males gain about the sperm competition probability with individual females. If males obtain no information from individual females, sperm numbers increase with q unless sperm limitation is high and one of the two competing ejaculates is strongly disfavoured. If males can distinguish between virgin and mated females, greater sperm allocation to virgins is favoured by high sperm limitation, high q, and by the second male's ejaculate being disfavoured. With high sperm limitation, sperm allocation to virgins increases and to mated females decreases with q at high q levels. With perfect information about female mating pattern, sperm allocation (i) to virgins that will mate again exceeds that to mated females and to virgins that will mate only once, (ii) to virgins that mate only once exceeds that for mated females if q is high and there is high second male disadvantage and (iii) to each type of female can decrease with q if sperm limitation is high, although the average allocation increases at least across low q levels. In general, higher sperm allocation to virgins is favoured by: strong disadvantage to the second ejaculate, high sperm limitation, high average risk and increased information (perceived risk). These conditions may apply in a few species, especially spiders.