Patterns Of Sperm Utilization Research Articles

Benefits of polyandry: Molecular evidence from field-caught dung beetles.

When females mate with multiple males, they set the stage for postcopulatory sexual selection via sperm competition and/or cryptic female choice. Surprisingly little is known about the rates of multiple mating by females in the wild, despite the importance of this information in understanding the potential for postcopulatory sexual selection to drive the evolution of reproductive behaviour, morphology and physiology. Dung beetles in the genus Onthophagus have become a laboratory model for studying pre- and postcopulatory sexual selection, yet we still lack information about the reproductive behaviour of female dung beetles in natural populations. Here, we develop microsatellite markers for Onthophagus taurus and use them to genotype the offspring of wild-caught females and to estimate natural rates of multiple mating and patterns of sperm utilization. We found that O.taurus females are highly polyandrous: 88% of females produced clutches sired by at least two males, and 5% produced clutches with as many as five sires. Several females (23%) produced clutches with significant paternity skew, indicating the potential for strong postcopulatory sexual selection in natural populations. There were also strong positive correlations between the number of offspring produced and both number of fathers and paternity skew, which suggests that females benefit from mating polyandrously by inciting postcopulatory mechanisms that bias paternity towards males that can sire more viable offspring. This study evaluates the fitness consequences of polyandry for an insect in the wild and provides strong evidence that female dung beetles benefit from multiple mating under natural conditions.

Post‐mating prezygotic barriers to gene exchange between hybridizing field crickets

Studies of sexual selection in speciation have traditionally focused on mate preference, with less attention given to traits that act between copulation and fertilization. However, recent work suggests that post-mating prezygotic barriers may play an important role in speciation. Here, we evaluate the role of such barriers in the field crickets, Gryllus firmus and Gryllus pennsylvanicus. Gryllus pennsylvanicus females mated with G. firmus males produce viable, fertile offspring, but when housed with both species produce offspring sired primarily by conspecifics. We evaluate patterns of sperm utilization in doubly mated G. pennsylvanicus females and find no evidence for conspecific sperm precedence. The reciprocal cross (G. firmus female × G. pennsylvanicus male) produces no progeny. Absence of progeny reflects a barrier to fertilization rather than reduced sperm transfer, storage or motility. We propose a classification scheme for mechanisms underlying post-mating prezygotic barriers similar to that used for premating barriers.

The Risk and Intensity of Sperm Ejection in Female Birds

The way females utilize the gametes of different males has important consequences for sexual selection, sexual conflict, and intersexual coevolution in natural populations. However, patterns of sperm utilization by females are difficult to demonstrate, and their functional significance remains unclear. Here, we experimentally study sperm ejection in the fowl Gallus gallus domesticus, where females eject preferentially the sperm of socially subordinate males. We study two measures of sperm ejection, (i) the probability that an ejaculate is ejected ("risk") and (ii) the proportion of semen ejected ("intensity"), and show that both measures are strongly nonrandom with respect to characteristics of the ejaculate, the male, and the female. Sperm ejection neutralized on average 80% of an ejaculate, and while larger ejaculates suffered a higher ejection risk, smaller ejaculates suffered more intense ejection. After controlling for ejaculate volume, we found socially subdominant males suffered higher ejection intensity. After controlling for male and ejaculate effects, we found ejection risk increased and intensity declined as females mated with successive males. Collectively, these results reveal that sperm ejection risk and intensity are at least partly actively caused by female behavior and generate independent selective pressures on male and ejaculate phenotypes.

The strength of postcopulatory sexual selection within natural populations of field crickets

Sperm competition and cryptic female choice are likely to exert strong postcopulatory sexual selection and may amplify or ameliorate selection acting via male mating success. However, relatively few studies have estimated the potential strength of postcopulatory sexual selection acting within natural populations. Field crickets in the genus Teleogryllus have been used extensively as laboratory models to study the evolution of polyandry, and the mechanisms of sperm competition and cryptic female choice. However, we have no knowledge of the extent of multiple mating or patterns of sperm utilization in natural populations of these crickets. We used microsatellite loci to examine the strength of postcopulatory sexual selection in Teleogryllus oceanicus and T. commodus. Genotyping of sperm within sperm storage organs revealed high levels of multiple mating by females in both species, but females utilized sperm from just 75% and 60% of their mates, respectively. Paternity was skewed toward a subset of fathers; skew was strongest in T. oceanicus and declined with the number of fathers represented in both species. Thus, postcopulatory sexual selection is strong in natural populations of both species and must be taken into account when estimating total sexual selection acting on these species. More generally, we argue that more effort should be made to measure the strength of postcopulatory sexual selection in other species, and to integrate episodes of pre- and postcopulatory selection, if we are to gain an accurate appreciation of the evolutionary consequences of sexual selection. Key words: cryptic female choice, paternity skew, polyandry, sperm competition, Teleogryllus commodus, Teleogryllus oceanicus. [Behav Ecol]

Variation in multiple paternity and sperm utilization patterns in natural populations of a simultaneous hermaphrodite land snail

Mating frequency has important implications for patterns of sexual selection and sexual conflict, and hence for issues such as the maintenance of genetic diversity and speciation. We assessed the level of multiple paternity and sperm utilization patterns in four natural populations of the simultaneous hermaphrodite land snail Arianta arbustorum using four polymorphic microsatellite loci. A total of 1088 offspring from 26 wild-caught snails were genotyped to determine the number of fathers siring each brood and paternity skew in succeeding clutches. Multiple paternity was detected in the offspring of all 26 mother snails examined with the contribution of two to six fathers. The four populations examined differed in the level of multiple paternity. Snails in the population with the highest density of adults showed the highest level of multiple paternity, whereas snails in the population with the lowest density exhibited the lowest value of multiple paternity. Highly skewed paternity patterns were found in the progeny of 15 (57.7%) of the 26 mother snails. The number and identity of fathers siring the offspring of single mothers also varied among successive clutches. Furthermore, genetic analyses indicate a low level of self-fertilization in one of the four populations.

Reproductive biology and mating conflict in the simultaneously hermaphroditic land snail Arianta arbustorum*

This review summarizes the present knowledge on the reproductive biology, mating system, sperm competition, sex allocation, and mating conflict in the simultaneously hermaphroditic land snail Arianta arbustorum (Linnaeus, 1758) (Helicidae). Field studies and controlled laboratory experiments indicate that mating is random with respect to shell size. However, subtle effects of inbreeding (reduced hatching success of eggs and viability of juveniles) and outbreeding were found. Individuals of A. arbustorum mate repeatedly with different partners and store viable sperm for more than one year. Spermatophore transfer is highly reciprocal, but the number of sperm they contain (800,000–4,000,000) is not necessarily equal. Snails need 3–4 weeks to replenish their autosperm reserves after a successful copulation. Sperm are monomorphic. However, there is considerable among-population—and to a minor extent—within-population variation in total sperm length. Sperm utilization patterns in double-mated individuals of A. arbustorum revealed striking differences among individuals. There is a huge variation in the structure of the spermatheca, which consists of 2–9 blind tubules. Different lines of evidence suggest that the snails might be able to store and expel sperm stored in single tubules and thus promote a selective fertilization of eggs (cryptic female choice). Maternal investment in eggs is considerable. Snails mated 1, 2, or 3 times showed that irrespective of the number of matings the individuals devoted >95% of the resources into the female function.

MALE RESIDENCY AND MATING PATTERNS IN A SUBSOCIAL SPIDER

Male mating strategies are often deployed with regard to female maturity and receptivity, possibly in response to sperm utilization patterns on the part of the female. We examined the pattern of male residency with females during the mating period of the subsocial spider Anelosimus cf. jucundus (Araneae, Theridiidae). We first examined patterns of male cohabitation with naturally occurring penul- timate instar and adult females in the field. Males were significantly more likely to be found in association with adult females, rather than with penultimate instar females. Penultimate instar and virgin adult females of known age were then placed into the field and monitored for residency by subsequently marked males. Males were, again, significantly more likely to be found in association with adult females, rather than with penultimate-instar females, although we were unable to determine if this pattern was due to differ- ential arrival or to differential retention of males at adult female web sites. Aspects of A. cf. jucundus natural history, including duration of male residency and frequency of mating in the field, are provided for the first time. We discuss the patterns of male residency in relation to predictions based on sperm utilization patterns by female A. cf. jucundus spiders.

Oocyte production and sperm utilization patterns in semi-fertile strains of Caenorhabditis elegans.

BackgroundCaenorhabditis elegans hermaphrodites are capable of producing hundreds of progeny. However, genetic and environmental factors can keep many animals from attaining their full reproductive potential. In these situations, efficient use of any functional gametes becomes more important for reproductive success. To learn about this aspect of C. elegans reproductive biology, we examined oocyte production and sperm utilization patterns in a unique collection of semi-fertile sperm function mutants.ResultsIn the mutants examined here, broods can be very small but sperm induced high levels of ovulation. Ovulation rates reach maximum levels between the first and second day of adulthood. Ovulations rates remain high during the reproductive period and gradually decline with age. These results further demonstrate a decoupling of the ability of sperm to fertilize oocytes and induce ovulation. We also observe that in our semi-fertile mutants the peak of successful fertilization events precedes the bulk of oocyte production. Mixing populations of functional and nonfunctional sperm under conditions without sperm competition also shows that functional sperm are utilized efficiently. Although overall brood size can be similar for different mutant strains, slight differences in the pattern of sperm utilization in these strains can lead to significant differences in resource utilization and population growth.ConclusionsThis study represents the first detailed description of oocyte and progeny production patterns over the entire reproductive period for wild-type and fertility impaired strains of C. elegans. The phenotype of our mutants provide an ideal system for studying sperm utilization patterns since they only affect one major process, the ability to fertilize oocytes. In semi-fertile mutants, the nature of the reproductive process and/or specific molecular mechanisms ensures that any functional sperm are utilized quickly. Only a fraction of the sperm produced by our semi-sterile mutants are functional as opposed to every sperm having a low but equal chance of fertilizing an oocyte. In addition to the number of progeny produced, the pattern of progeny production can have an important influence on the dynamics of population growth.

The Genetics of Reproductive Isolation: A Retrospective and Prospective Look with Comments on Ground Crickets

An intriguing aspect of the current renaissance in investigations of the genetics of reproductive isolation is that it has been dominated by studies that resemble work done in the 1930s, 1940s, and 1950s. The dominant model organism (Drosophila), research approaches, and traits of interest (sterility and inviability of hybrids) all harken back to this earlier era. Herein, we explore the factors that led to a rebirth of interest in the genetics of reproductive isolation and to the adoption of the approaches of an earlier generation of biologists. At the same time, we appeal for more intensive investigations of traits that reproductively isolate closely related species, inclusion of a greater range of organisms in studies of reproductive isolation, and focus on a broader range of questions surrounding speciation. We end with a description of ongoing quantitative trait loci (QTL) studies of conspecific sperm precedence in the ground crickets Allonemobius fasciatus and Allonemobius socius. We have found several QTL with large effects on variance in patterns of sperm utilization in backcross females. Moreover, some QTL have an antagonistic effect on conspecific sperm, a finding that lends support to the hypothesis that rapid evolution of conspecific sperm precedence is a by-product of sexual conflict.

Sperm Displacement in the Yellow Dung Fly, Scatophaga stercoraria: An Investigation of Male and Female Processes.

Despite the ubiquity with which patterns of sperm utilization have been studied, the mechanisms underlying fertilization in insects are far from clear. One well-studied system is the yellow dung fly, in which the last male's ejaculate is thought to displace rival sperm from the female's sperm stores. Here we follow the movement of the copulating male's ejaculate through the female's reproductive tract using males labeled with different radioisotopes. We find that males ejaculate into the bursa copulatrix and that male-1 sperm are displaced from the spermathecae during copulation. The increase in male-2 ejaculate in the spermathecae matches the pattern of male-2 fertilization gain, indicating that only spermathecal sperm are utilized at fertilization. Previously we have analyzed this system with a direct model of sperm displacement in which the male displaces rival sperm from the spermathecae. The data, and morphology of the female, clearly preclude such a mechanism. Here we contrast this model with a new indirect model, in which the female facilitates displacement by exchange of sperm from the bursa copulatrix to the spermathecae. The two models give equivalent fits to the observed sperm utilization patterns because the rate of sperm transfer into the bursa copulatrix greatly exceeds the rate of sperm exchange with the spermathecae so that the concentration of the first male's sperm in the bursa remains considerably lower than that of the second male. These analyses provide a quantitative attempt to incorporate female processes into the analysis of sperm utilization patterns in insects.

Sperm Displacement in the Yellow Dung Fly, Scatophaga stercoraria: An Investigation of Male and Female Processes

Despite the ubiquity with which patterns of sperm utilization have been studied, the mechanisms underlying fertilization in insects are far from clear. One well‐studied system is the yellow dung fly, in which the last male's ejaculate is thought to displace rival sperm from the female's sperm stores. Here we follow the movement of the copulating male's ejaculate through the female's reproductive tract using males labeled with different radioisotopes. We find that males ejaculate into the bursa copulatrix and that male‐1 sperm are displaced from the spermathecae during copulation. The increase in male‐2 ejaculate in the spermathecae matches the pattern of male‐2 fertilization gain, indicating that only spermathecal sperm are utilized at fertilization. Previously we have analyzed this system with a direct model of sperm displacement in which the male displaces rival sperm from the spermathecae. The data, and morphology of the female, clearly preclude such a mechanism. Here we contrast this model with a new indirect model, in which the female facilitates displacement by exchange of sperm from the bursa copulatrix to the spermathecae. The two models give equivalent fits to the observed sperm utilization patterns because the rate of sperm transfer into the bursa copulatrix greatly exceeds the rate of sperm exchange with the spermathecae so that the concentration of the first male's sperm in the bursa remains considerably lower than that of the second male. These analyses provide a quantitative attempt to incorporate female processes into the analysis of sperm utilization patterns in insects.

Multiple mating by females is not dependent on body size in the salamander Desmognathus ochrophaeus

AbstractMale mate choice for particular "classes" of females may be devalued if chosen females are more likely to mate with multiple partners (thus precipitating sperm competition). Larger females carry greater numbers of eggs available for fertilization in the plethodontid salamander Desmognathus ochrophaeus, and are chosen by males in simultaneous mate-choice tests. We found no difference in mating frequency between 12 large females and 12 smaller females across 576 male-female encounters. Given limited published data on patterns of sperm utilization in this salamander, we conclude that male choice of more fecund partners may be advantageous even in the face of multiple mating by females and resultant sperm competition. Studies of natural populations of salamanders are required to confirm this conclusion.

Determinants of paternity in the milkweed leaf beetle

Males and females of the milkweed leaf beetle mate for up to 2.5 d in the field; copulation is interspersed with mounted courtship behavior and periods of passive riding on the female's back. In 1985, females mated with up to 10 different males in Bridgeport, New York, and matings averaged 0.75±0.04 (SE) d in duration. Sperm utilization patterns are complex in the milkweed leaf beetle. In the laboratory, mating duration, mating order and the duration of the gap between matings affected paternity. The second male's sperm predominated when a female's two consecutive matings were of equal duration (but were long: 45 h each) or when they were intermediate in duration (15 h each) with a 5 day gap between the two matings. The mechanism of sperm predominance appears to be one of time-dependent sperm removal and replacement. Neither relative nor absolute size of males affected the extent to which they superceded the sperm of rivals. Electrophoretic analysis of paternity at 6 polymorphic loci showed that offspring of at least eight out of 11 mating pairs pairs collected in the field at the end of the 1984 breeding season were sired by more than one male. At least seven of the 11 families produced some offspring that were sired by the female's most recent mate in the field and in no case was the collected male completely excluded from paternity. In a greenhouse plot, males climbed off females' backs a mean of 1.1±0.3 h before oviposition. Females did not oviposit with males on their backs and did not oviposit sooner when males were removed than when males were allowed to remain mounted, indicating that males don't keep females from ovipositing until they can achieve sperm predominance. The close concordance between male disembarkment and oviposition suggests that males remain with females beyond the time when they have superceded the sperm of their prior mates, possibly to guard them from rival males. Although the prolonged mating association of the milkweed leaf beetle cannot be separated into discrete copulatory and guarding phases, the results of this study suggest that prolonged mating enables males both to remove and replace the sperm of the females' prior mates with their own sperm and to prevent females from remating prior to oviposition.

Estimating the degree of sperm precedence in laboratory mating experiments: a maximum likelihood method.

Allozyme polymorphisms have been used frequently in laboratory mating experiments to study patterns of sperm utilization in multiply mated females. In some instances, due either to chance or to design, there is a diagnostic difference between male genotypes that allows unambiguous assignment of paternity. In other instances, there is some overlap in allelic composition of males, so that attribution of paternity is often uncertain. This paper presents a statistical method for analyzing data of the second sort obtained from twice-mated females, based on the principle of maximum likelihood. The method allows the estimation of a mating parameter, psi the frequency with which sperm from the first male fertilizes the female's eggs. Various hypotheses about the null value of psi may be tested by a likelihood ratio test statistic. Also presented is a method of testing for homogeneity in psi values across different broods produced by the same female.

Determinants of mating success in the golden hamster ( Mesocricetus auratus): Social dominance and mating tactics under seminatural conditions

We tested the hypothesis that high social status leads to high levels of copulatory behaviour and increased number of offspring in hamsters. When paired with albino female golden hamsters, males of three genotypic strains showed differences in the frequency and temporal patterning of some measures of copulatory behaviour but did not differ in general fertilization success. The results of two-male, one-female tests in which mating order and ejaculation frequencies were controlled indicated only relatively small differences in differential fertilizing capacity among these genotypes. Males of the genotypic strains displayed an equal probability of achieving alpha status in three-male, one-female competitive mating tests in which animals were habituated to semi-natural enclosures. Alpha males often slept in the female's nest box the night before she became receptive, were the first to mate on the following morning, achieved higher scores for all measures of sexual behaviour including ejaculation frequency and subsequently sired more young than did lower ranking males. However, the differential reproductive success of alpha males was not simply a function of higher ejaculation scores since they obtained more than twice as many young per ejaculation as subordinate males. Alpha males continued to copulate with long intromissions after exhausting their supply of ejaculates. Although females mated with several males, mating preferences were evidenced by their flank-gland and vaginal marking patterns on the day before receptivity and in their initial choice of mates during tethered male tests. The behaviour of alpha males is consistent with previous findings regarding the effects of mating order and prolonged copulation on sperm competition and suggests that sperm utilization patterns and mating tactics have coevolved.