Male Fertilization Success Research Articles

Dietary carotenoid availability, sexual signalling and functional fertility in sticklebacks

In species where males express carotenoid-based sexual signals, more intensely coloured males may be signalling their enhanced ability to combat oxidative stress. This may include mitigating deleterious oxidative damage to their sperm, and so be directly related to their functional fertility. Using a split-clutch in vitro fertilization technique and dietary carotenoid manipulation, we demonstrate that in non-competitive fertilization assays, male three-spined sticklebacks (Gasterosteus aculeatus) that are fed higher (but biologically relevant) levels of carotenoids had a significantly increased fertilization success, irrespective of maternal carotenoid intake. Furthermore, within diet groups, a male's fertilization success was positively related to the expression of his carotenoid-based nuptial coloration, with more intensely coloured males having higher functional fertility. These data provide, to our knowledge, the first demonstration that dietary access to carotenoids influences fertilization success, and suggest that females could use a male's nuptial coloration as an indicator of his functional fertility.

SEXUAL SELECTION, MULTIPLE MALE ORNAMENTS, AND AGE- AND CONDITION-DEPENDENT SIGNALING IN THE COMMON YELLOWTHROAT

In many animals, sexual selection has resulted in complex signaling systems in which males advertise aspects of their phenotypic or genetic quality through elaborate ornamentation and display behaviors. Different ornaments might convey different information or be directed at different receivers, but they might also be redundant signals of quality that function reliably at different times (ages) or in different contexts. We explored sexual selection and age- and condition-dependent signaling in the common yellowthroat (Geothlypis trichas), a sexually dichromatic warbler with two prominent plumage ornaments--a melanin-based, black facial "mask" and carotenoid-based, UV-yellow "bib." In a three-year study, variance among males in the number of social (M(w)) and extra-pair (M(e)) mates generated strong sexual selection on mask and bib attributes. Some traits (mask size, bib yellow brightness) were correlated with male age and did not experience selection beyond age-related increases in M(w) and M(e). Other traits showed age-specific (bib size) or age-reversed (ultraviolet brightness) patterns of selection that paralleled changes in the information-content of each ornament. The components of male fitness generating selection in young versus old males were distinct, reflecting different sources of variation in male fertilization success. Age- and context-dependent changes in the strength, direction, and target of selection may help explain the maintenance of multiple ornaments in this and other species.

Sperm competitiveness in frogs: slow and steady wins the race.

When sperm compete to fertilize available ova, selection is expected to favour ejaculate traits that contribute to a male's fertilization success. While there is much evidence to show that selection favours increased numbers of sperm, only a handful of empirical studies have examined how variation in sperm form and function contributes to competitive fertilization success. Here, we examine selection acting on sperm form and function in the externally fertilizing myobatrachid frog, Crinia georgiana. Using in vitro fertilization techniques and controlling for variation in the number of sperm contributed by males in competitive situations, we show that males with a greater proportion of motile sperm, and motile sperm with slower swimming velocities, have an advantage when competing for fertilizations. Sperm morphology and the degree of genetic similarity between putative sires and the female had no influence on competitive fertilization success. These unusual patterns of selection might explain why frog sperm typically exhibit relatively slow swimming speeds and sustained longevity.

Sexual selection and the rodent baculum: an intraspecific study in the house mouse (Mus musculus domesticus)

The rapid divergence of genitalia is a pervasive trend in animal evolution, thought to be due to the action of sexual selection. To test predictions from the sexual selection hypothesis, we here report data on the allometry, variation, plasticity and condition dependence of baculum morphology in the house mouse (Mus musculus domesticus). We find that that baculum size: (a) exhibits no consistent pattern of allometric scaling (baculum size being in most cases unrelated to body size), (b) exhibits low to moderate levels of phenotypic variation, (c) does not exhibit phenotypic plasticity in response to differences in perceived levels of sexual competition and (d) exhibits limited evidence of condition dependence. These patterns provide only limited evidence in support of the sexual selection hypothesis, and no consistent support for any particular sexual selection mechanism; however, more direct measures of how genital morphology influences male fertilization success are required.

Courtship raises male fertilization success through post-mating sexual selection in a spider.

Courtship is well known for its positive effects on mating success. However, in polyandrous species, sexual selection continues to operate after copulation. Cryptic female choice is expected under unpredictable mating rates in combination with sequential mate encounters. However, there are very few accounts of the effects of courtship on cryptic female choice, and the available evidence is often correlative. Mature Argiope bruennichi females are always receptive and never attack or reject males before mating, although sexual cannibalism after mating occurs regularly. Still, males usually perform an energetic vibratory display prior to copulation. We tested the hypothesis that beneficial effects of courtship arise cryptically, during or after mating, resulting in increased paternity success under polyandry. Manipulating courtship duration experimentally, we found that males that mated without display had a reduced paternity share even though no differences in post-copulatory cannibalism or copulation duration were detected. This suggests that the paternity advantage associated with courtship arose through female-mediated processes after intromission, meeting the definition of cryptic female choice.

Large spermatophores reduce female receptivity and increase male paternity success in the almond moth, Cadra cautella

The size of a male's reproductive investment may have profound consequences for female mating frequency and male fitness. Male ejaculate size may affect female fecundity and fertility, while large ejaculates may confer an advantage for males in both avoiding and engaging in sperm competition. We explored experimentally the effect of male ejaculate size on female receptivity and male fertilization success, in the largely monandrous almond moth. Females received either a large or small first spermatophore, and were then given the opportunity to remate with another male that also provided a large or small ejaculate. We examined the effect of spermatophore size on female postmating receptivity, likelihood of remating and reproductive output. For males, we examined the effect that spermatophore size and mating order had on subsequent paternity success. Females that received a small first ejaculate were both more likely to remate (with mated males) and remated sooner than females that received a large first ejaculate. Furthermore, females that remated were also more likely to commence calling behaviour following their first mating, but there were no effects of spermatophore size on female reproductive output. For a male, however, if his female remated, the size of the spermatophore he transferred had important fitness consequences. Second-mating males suffered a paternity cost when competing against a rival that provided a large spermatophore. We propose that the enlarged spermatophore transferred by virgin males explains the low remating rate in this species, and may suggest a more polyandrous past for the almond moth, potentially shaped by sexual conflict.

Prudent male mate choice under perceived sperm competition risk in the eastern mosquito fish

In contrast to what is known about adaptive mate choice in females, we know far less about how fluctuating reproductive costs might affect male mate choice. In many species, sperm competition can have a direct bearing on male fertilization success, and choosy males should be expected to respond adaptively to the perceived cost of sperm competition and to adjust their mate preferences accordingly. Here, we conducted a series of experiments investigating male mate choice under sperm competition risk in the eastern mosquito fish, Gambusia holbrooki. We tested male association preferences before and after manipulating their perceptions of sperm competition risk associated with initially preferred and nonpreferred females. We found that individuals were consistent in their preferences if they did not have the opportunity to witness other males associating with the initially preferred female. By contrast, males spent significantly less time with initially preferred females if, in the interim, she had been seen in the vicinity of another male. A similar opportunity to observe the initially nonpreferred female with another male had no effect on subsequent male mate choice. Our results suggest that choosy males may be capable of adjusting their preferences in response to shifts in their perception of sperm competition risk. Key words: eavesdropping, intrasexual competition, mate choice copying, Poeciliidae, sexual selection. [Behav Ecol]

POSTCOPULATORY FEMALE CHOICE INCREASES THE FERTILIZATION SUCCESS OF NOVEL MALES IN THE FIELD CRICKET,GRYLLUS VOCALIS

Although recent studies have demonstrated that female crickets prefer novel males to previous mates, the relative contribution of pre- and postcopulatory behaviors to this advantage remain unknown, as do the reproductive consequences to males. I paired females either with previous or novel mates, and recorded the latency to mating and the time after mating at which the female removed the male's spermatophore, terminating sperm transfer. Females that mated with familiar males removed their spermatophores sooner than females that mated with novel males. Females paired with novel males also mated more quickly than females paired with familiar males, but this difference was not statistically significant. A molecular-based paternity analysis was used to determine whether the postcopulatory preference of females for novel males influences a male's fertilization success. Females were assigned to either mate three times with the same male and then once with a novel male, or four times with four different males. The paternity of the last male was higher when the female previously had mated repeatedly with the same male than when she had mated previously with different males. These results suggest that female spermatophore removal behavior influences male paternity such that novel males receive a fertility benefit.

EVOLUTIONARY REDUCTION IN TESTES SIZE AND COMPETITIVE FERTILIZATION SUCCESS IN RESPONSE TO THE EXPERIMENTAL REMOVAL OF SEXUAL SELECTION IN DUNG BEETLES

Sexual selection is thought to favor the evolution of secondary sexual traits in males that contribute to mating success. In species where females mate with more than one male, sexual selection also continues after copulation in the form of sperm competition and cryptic female choice. Theory suggests that sperm competition should favor traits such as testes size and sperm production that increase a male's competitive fertilization success. Studies of experimental evolution offer a powerful approach for assessing evolutionary responses to variation in sexual selection pressures. Here we removed sexual selection by enforcing monogamy on replicate lines of a naturally polygamous horned beetle, Onthophagus taurus, and monitoring male investment in their testes for 21 generations. Testes size decreased in monogamous lines relative to lines in which sexual selection was allowed to continue. Differences in testes size were dependent on selection history and not breeding regime. Males from polygamous lines also had a competitive fertilization advantage when in sperm competition with males from monogamous lines. Females from polygamous lines produced sons in better condition, and those from monogamous lines increased their sons condition by mating polygamously. Rather than being costly for females, multiple mating appears to provide females with direct and/or indirect benefits. Neither body size nor horn size diverged between our monogamous and polygamous lines. Our data show that sperm competition does drive the evolution of testes size in onthophagine beetles, and provide general support for sperm competition theory.

MALE GENETIC QUALITY AND THE INEQUALITY BETWEEN PATERNITY SUCCESS AND FERTILIZATION SUCCESS: CONSEQUENCES FOR STUDIES OF SPERM COMPETITION AND THE EVOLUTION OF POLYANDRY

Studies of postcopulatory sexual selection typically estimate a male's fertilization success from his paternity success (P2) calculated at hatching or birth. However, P2 may be affected by differential embryo viability, thereby confounding estimations of true fertilization success (F2). This study examines the effects of variation in the ability of males to influence embryo viability upon the inequality between P2 and F2. It also investigates the consequences of this inequality for testing the hypothesis that polyandrous females accrue viability benefits for their offspring through facilitation of sperm competition (good-sperm model). Simulations of competitive mating trials show that although relative measures of male reproductive success tend to underestimate the strength of underlying good-sperm processes, good-sperm processes can be seriously overestimated using P2 values if males influence the viability of the embryos they sire. This study cautions the interpretation of P2 values as a proxy for fertilization success or sperm competitiveness in studies of postcopulatory sexual selection, and highlights that the good-sperm hypothesis needs empirical support from studies able to identify and separate unequivocally the males' ability to win fertilizations from their ability to influence the development of embryos.

Factors predicting male fertilization success in an external fertilizer

In postcopulatory sexual selection both sperm competition and cryptic female choice are considered to be important selective agents, but their relative importance for male fertilization success has received little attention. We tested whether sperm quality, male spawning coloration, male heterozygosity, and genetic overlap with the female explained a male’s fertilization success in controlled in vitro fertilization competition trials between equal numbers of sperm from pairs of male Arctic charr (Salvelinus alpinus), an external fertilizer. Offspring were genotyped to determine each males’ share of paternity. The velocity of a male’s sperm relative to the velocity of the competing male’s sperm was the best predictor of male fertilization success. Yet, sperm velocity was not related to spawning coloration or male heterozygosity. In fact, the most brightly colored male in a pair had the lowest fertilization probability. This could result from cryptic female choice for pale males, but might rather be a result of paler males producing more competitive sperm than more colored males. Furthermore, the more microsatellite alleles a male shared with the female relative to the competing male, the higher fertilization success he had. We argue that this latter may be an effect of assortative cryptic female choice, which might prevent hybridization with sympatric Arctic charr morphs or one form of kin selection.

Size-dependent mating strategies and the risk of cannibalism

The role of sexual selection in determining the nature and direction of sexual size dimorphism may depend upon the timing of sexual selection, and this may also influence the variation in male size. For example, selection through sperm competition favours smaller males in the highly sexually size dimorphic orb-weaving spider Nephila edulis, whereas larger males are better able to exclude their smaller rivals from the central hub of the web where mating takes place. We investigate experimentally the role of body size and hub tenure in determining male fertilization success when males of different sizes compete for a single female over a 24-h period that includes a period of darkness. Our results confirm that small and large males obtain similar paternity share but that, in contrast with previous studies, hub tenure does not translate into greater paternity share. Unexpectedly, smaller males are at greater risk of postmating sexual cannibalism than larger males, suggesting that natural selection through sexual cannibalism may place a lower limit on male size.

GAMETE TRAITS INFLUENCE THE VARIANCE IN REPRODUCTIVE SUCCESS, THE INTENSITY OF SEXUAL SELECTION, AND THE OUTCOME OF SEXUAL CONFLICT AMONG CONGENERIC SEA URCHINS

Sea-urchin species differ in susceptibility to sperm limitation and polyspermy, but the influences of gamete traits on reproductive variance, sexual selection, and sexual conflict are unknown. I compared male and female reproductive success of two congeners at natural densities in the sea. The eggs of the species occurring at higher densities, Strongylocentrotus purpuratus, require higher sperm concentrations for fertilization but are more resistant to polyspermy compared to S. franciscanus. Both species show high variance in male fertilization success at all densities and high variance in female success at low densities, but they differ in female variance at high densities, where only S. franciscanus shows high female variance. The intensity of sexual selection based on Bateman gradients is high in males of both species, variable in S. franciscanus females, and low in S. purpuratus females. Strongylocentrotus franciscanus females experience sexual selection at low densities and sexual conflict at high densities. Strongylocentrotus purpuratus may rarely experience sperm limitation and may have evolved to ameliorate sexual conflict. This reduces the variance in female fertilization, providing females with more control over fertilization. Sperm availability influences sexual selection directly by determining sperm-egg encounter probabilities and indirectly through selection on gamete traits that alter reproductive variances.

Mating Competition in Colorado Potato Beetles (Coleoptera: Chrysomelidae) Does Not Show a Cost of Insecticide Resistance

Resistance to insecticides is often linked with fitness costs. Although costs affecting lifetime reproduction in females will have the greatest effect on resistance evolution, fertilization costs in males, through less vigorous mating behavior or less effective sperm in resistant individuals, will slow the spread of resistance. We used a sterile male technique to measure the relative mating competitiveness of Colorado potato beetles, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), resistant or susceptible to imidacloprid. We showed that 5,000 Krad from a cesium-137 source was sufficient to sterilize male beetles. We tested mating competitiveness by placing a single resistant and a single susceptible male beetle with a virgin susceptible female in circular acetate enclosures surrounding potted potato plants, and we observed frequency of mating or mounting with each male and subsequent fertilization success. Resistant males mate just as often as susceptible males during 24-h competitive interactions. Hatch rate was correlated with the proportion of matings or mounts observed with the nonirradiated male, but no effect of the first or last male, nor of resistance on fertilization success was observed, and resistance does not seem to incur a behavioral or sperm-competitive fertilization cost.

Wing morph- and age-related differences in fertilization success of adult males of a flightless bug, Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae)

The aim of the present study was to test the hypothesis that short-winged (brachypterous) and long-winged (macropterous) adult males of a flightless bug Pyrrhocoris apterus differ in fertilization success. For this purpose, 5, 10 and 28 days old brachyp- terous and macropterous males were mated for the same period of time with reproductively active 5 days old brachypterous females. The average hatchability of five egg batches of these females was used as a measure of the fertilization success of the males. The results revealed significantly higher hatchability of the eggs laid by females that copulated with 5 or 10 days old brachypterous males than with same-aged macropterous males. In contrast, the average hatchability of eggs of females that copulated with 28 days old brachypterous males was significantly lower than of those mated with same-aged macropterous males. It is the first report of wing morph- and age-related differences in fertilization success of males in insects with a non-functional wing-polymorphism. The possible relationship between wing- and age-related differential fertilization and the mating success of P. apterus males, and differ- ences in the amount of secretion transferred from their accessory glands into the reproductive tract of females during copulation, is discussed.

A mechanism for cryptic female choice in chinook salmon

Female mate choice after copulation or spawning is cryptic when a female differentially influences the fertilization success of sperm from different males. We tested whether ovarian fluid could act as a potential mechanism of cryptic female choice (CFC) in chinook salmon (Oncorhynchus tshawytscha) by comparing how ovarian fluid from each of 7 females affected the sperm behavior of 11 different males. Using computer-assisted sperm analysis, we measured sperm velocity, motility, longevity, and linearity from the ejaculates of each male activated in the ovarian fluid from each female. Mean sperm swimming speed, path trajectory, and longevity differed significantly among males, and within males depended on the female’s ovarian fluid in which it was activated. Most important, the pattern of within-male variation in these traits also varied significantly among males in response to different females’ ovarian fluids. As sperm velocity is known to be a prime determinant of fertilization success in externally fertilizing fishes. This finding suggests that variation in the composition of female ovarian fluid may be a mechanism for CFC, whereby females differentially enhance the swimming speed of sperm from different males. Thus, female ovarian fluid can alter relative male fertilization success when there is intense sperm competition, as there is in this and other group spawning fish species. Key words: chinook salmon, cryptic female choice, Oncorhynchus tshawytshca, ovarian fluid, sperm traits, sperm velocity. [Behav Ecol]

Dual function of seminal substances for mate guarding in a ground beetle

Males of internally fertilizing animals often produce ejaculates consisting of various substances in addition to sperm. Seminal substances can inhibit female remating through physical blocking of the female genitalia or by physiological induction of the female refractory period. We demonstrated that the seminal substances of the ground beetle Leptocarabus procerulus serve as both physical (i.e., mating plugs) and physiological (i.e., substances inducing female refractory behavior) devices for mate guarding. Although females counteract these functions via expulsion of the plug and the delay of the occurrence of refractory behavior, the interplay of these 2 functions can be compensatory and consistently lowers the female remating rate during a postmating period that is important for male fertilization success. Such interplay of 2 defensive strategies may be a male adaptation against female resistance, as predicted by the hypothesis that multiple functions in seminal substances are a historical outcome of an arms race between males and females. Our findings highlight the importance of sexual conflict in the evolution of complex seminal substances. Key words: accessory gland protein, mating plug, sexual conflict, sexual selection, sperm competition. [Behav Ecol]

Pedigree and mating system analyses in a western larch (Larix occidentalis Nutt.) experimental population

•The mating pattern and gene flow in a western larch (Larix occidentalis Nutt.) experimental population was studied with the aid of microsatellite markers and a combination of paternity-mating system analysis. The commonly difficult to assess, male gametic contribution was determined with 95% confidence and its impact on genetic gain and diversity was determined. • Male fertility success rate ranged between 0 and 11%. Male reproductive output parental imbalance was observed with 50% of the pollen being produced by the top 5% of males while the lower 39% males only produced 10% of the pollen. • A significant difference was observed between male effective population size (genetic diversity) estimates from paternity assignment compared to those based on population’s census number (21 vs. 41); however, this difference did not affect estimates of genetic gain. • A total of 221 full-fib families were identified (sample size range: 1‐8) and were nested among the studied 14 seed-donors. • A combination of paternity-mating system analysis is recommended to provide a better insight into seed orchards’ mating dynamics. While pollen flow tends to inflate mating system’s outcrossing rate, the paternity analysis effectively determined the rate and magnitude of contamination across receptive females.

Effectiveness of territorial polygyny and alternative mating strategies in northern fur seals, Callorhinus ursinus

We conducted a 6-year longitudinal behavioral and genetic investigation of a highly polygynous pinniped, the northern fur seal (Callorhinus ursinus), to determine the contribution of terrestrial polygyny to male fertilization success and to assess the occurrence of alternative mating strategies. Genetic samples from 37 adult males, 50 adult females, and 85 pups were collected and genotyped using five polymorphic microsatellite loci. Pup paternity was assigned using Cervus 2.0 at 99% confidence level. Paternity of 83 pups (98%) was assigned to terrestrial males who held territories or stayed temporarily in the study area during the breeding season when fertilization occurred. For 56 pups of which attendance records of their mothers were available, paternity of 45 pups (80%) was assigned to the associate males in whose territory their mothers stayed during the perioestrus period. In addition to defending breeding territories, territorial males have often been observed attempting to forcibly abduct adult females from adjacent territories (female stealing): We observed a total of 95 such cases, in which the stealers had significantly fewer females than the territorial males from whose territories they stole females. Our results indicate that terrestrial resource-defense polygyny is the major mating system in this species and that nonassociated paternity occurs mostly as a result of alternative mating strategies of less successful males. Male northern fur seals thus appear to adopt conditional alternative strategies that depend on their current social status to maximize their life-time reproductive success.

Parasperm: morphological and functional studies on nonfertile sperm

Sperm polymorphism, a phenomenon in which more than one type of sperm is produced within a species, occurs widely in animals from invertebrates to vertebrates. Sperm in this phenomenon can be categorized into fertile sperm and nonfertile sperm on the basis of fertilization ability. Nonfertile sperm can be further classified into parasperm and aberrant deformed sperm. Parasperm are sperm produced through a constant developmental process along with normal fertile eusperm, and they are readily distinguished from deformed sperm, which are irregularly crippled by unpredictable errors at certain stages during spermatogenesis. Sperm identified as parasperm occur widely in invertebrates but are presently quite limited in vertebrates. This may be the result of the deficiency both of studies on parasperm and of clear criteria to identify parasperm in vertebrates. Some vertebrates show unique spermatogenesis, such as symplastic spermatid and semicystic spermatogenesis. Thus, parasperm must be identified by comparing cells in each cyst and in semen, because irregularly shaped cells in the seminal duct could be either parasperm or normal spermatids. Although parasperm are identified by clear criteria in vertebrates, only in cottoid fishes to date, it is possible for parasperm to be discovered in other vertebrates. Recently, roles related to sperm competition have been reported in several species (e.g., the marine cottoid fish Hemilepidotus gilberti), and, with some of them, parasperm production is influenced by an intraspecific factor such as a sex ratio or the density of a population. Sperm competition is one of the important candidates for influencing evolution of parasperm functions, but not all parasperm seem to have a relation to sperm competition. Parasperm function may relate to the ecological conditions of each species that produces parasperm. Studies on parasperm function will be advanced by an ecological approach concerning male fertilization success as well as cytological investigation for parasperm.