THE LIKELIHOOD OF SPERM COMPETITION IN MANATEES-EXPLAINING AN APPARENT PARADOX

Florida manatees ( Trichechus manatus latirostris ) are promiscuous, with multiple males mating with individual females. This suggests manatees are sperm competitors. Surprisingly, manatee testes are not relatively large. For adult males in non-winter, testicular size is approximately twice what is expected, based on allometry, for "typical" ( i. e. , non-sperm competitor) male mammals of similar size; for these manatees, combined testicular weight represents 0.19% of the body weight ( n = 27 manatees). Testicular weight was generally largest in manatees older than 7 yr in non-winter. Testicular size of some sperm competitors is as much as an order of magnitude (or more) larger than expected in a "typical" species. Perhaps in compensation for the testes not being remarkably large, the seminal vesicles of mature manatees may be larger than the testes. Production of notably large volumes of seminal fluid characterizes sperm competitor primate species and may have positive energy consequences for species such as the manatee that have extremely low metabolic rates. Another possible explanation for the observed relationship between testicular mass and body mass in manatees is that selection for a greatly expanded hindgut and extremely dense, heavy integument could make the body mass of manatees "artificially" high, and the relative testicular mass "artificially" low.     

INFERENCE OF SPERM COMPETITION FROM BROODS OF FIELD-CAUGHT DROSOPHILA

In field studies of multiple mating and sperm competition there typically is no experimental control over the number of times that a female mates, the interval between matings, or the genetic identity of multiple fathers contributing to a brood. Irrespective of this complexity, high-resolution molecular markers can be used to assign paternity with considerable confidence. This study employed two highly heterozygous microsatellite loci to assess multiple paternity and sperm displacement in a sample of broods taken from a natural population of Drosophila melanogaster. The large number of alleles present at each of the loci makes it difficult to derive explicit maximum-likelihood estimates for multiple paternity and sperm displacement from brood samples. Monte Carlo simulations were used to estimate maximum-likelihood parameters for the distribution of female remating frequency and the proportion of offspring sired by the second or subsequent mating males. Estimates were made based on genotypes scored at two distinct marker loci because they were found to give statistically homogeneous results. Fitting a Poisson distribution of number of matings, the mean number of males mated by a female was 1.82. The sperm displacement parameter estimated from doubly mated females were 0.79 and 0.86 for the two loci (0.83 for the joint estimate). The overall probability that a multiply mated female will be misclassified as singly mated was only 0.006, which indicates that microsatellites can provide excellent resolution for identifying multiple mating. In addition, microsatellites can be used to generate relatively precise estimates of sperm precedence in brood-structured samples from a natural population.     

ADAPTIVE PHENOTYPIC PLASTICITY IN GROWTH,DEVELOPMENT, AND BODY SIZE IN THE YELLOW DUNG FLY

Life-history theory predicts that age and size at maturity of organisms should be influenced by time and food constraints on development. This study investigated phenotypic plasticity in growth, development, body size, and diapause in the yellow dung fly, Scathophaga stercoraria. Full-sib families were allowed to develop under predator-free field conditions. The time before the onset of winter was varied and each brood was split into three environments differing in the amount of dung a set number of larvae had as a resource. When resources were abundant and competition was minimal, individuals of both sexes grew to larger body sizes, took longer time to mature, and were able to increase their growth rates to attain large body sizes despite shorter effective development periods later in the season. In contrast, limited larval resources and strong competition constrained individuals to mature earlier at a smaller adult size, and growth rates could not be increased but were at least maintained. This outcome is predicted by only two life-history optimality models, which treat mortality due to long development periods and mortality due to fast growth as independent. Elevated preadult mortality indicated physiological costs of fast growth independent of predation. When larval resources were limited, mortality increased with heritable variation in development time for males, and toward the end of the season mortality increased as larval resources became more abundant because this induced longer development periods. Sexual and fecundity selection favoring large body size in this species is thus opposed by larval viability selection favoring slower growth in general and shorter development periods when time and resources are limited; this overall combination of selective pressures is presumably shaping the reaction norms obtained here. Flexible growth rates are facilitated by low genetic correlations between development time and body size, a possible consequence of selection for plasticity. Heritable variation was evident in all traits investigated, as well as in phenotypic plasticity of these traits (genotype X interactions). This is possibly maintained by unpredictable spatiotemporal variation in dung abundance, competition, and hence selection.     

SPERM COMPETITION SELECTS BEYOND RELATIVE TESTES SIZE IN BIRDS

Sperm morphology varies considerably across taxa, and postcopulatory sexual selection is thought to be one of the main forces responsible for this diversity. Several studies have investigated the effects of the variation in sperm design on sperm function, but the consequences of variation in sperm design on testis morphology have been overlooked. Testes size or architecture may determine the size of the sperm they produce, and selection for longer sperm may require concomitant adaptations in the testes. Relative testes size differs greatly between species and is often used as an index of sperm competition, but little is known about whether larger testes have more sperm-producing tissue or produce sperm at a faster rate. Using a comparative approach in New World Blackbirds (Icteridae), we found (1) a strong link between testis histology and sperm length, suggesting selection on testis architecture through selection on sperm size, and (2) that species under intense sperm competition had a greater proportion of sperm-producing tissue within their testes. These results support the prediction that sperm competition fosters adaptations in reproductive organs that extend beyond testes size, and raise questions about the trade-offs influencing reproductive investment.     

SPERM COMPETITIVE ABILITY AND INDICES OF LIFETIME REPRODUCTIVE SUCCESS

Understanding the selection pressures shaping components of male reproductive success is essential for assessing the role of sexual selection on phenotypic evolution. A male's competitive reproductive success is often measured in sequential mating tests by recording P1 (first mating male) and P2 (second mating male) paternity scores. How each of these scores relates to a male's overall fitness, for example, lifetime reproductive success is, however, not known. This information is needed to determine whether males benefit from maximizing both P1 and P2 or by trading off P1 against P2 ability. We measured P1, P2, and an index of lifetime reproductive success (LRS_i, a male's competitive reproductive success measured over 12 days) for individual male Drosophila melanogaster. We found no evidence for phenotypic correlations between P1 and P2. In addition, whereas both P1 and P2 were associated with relative LRS_i, only P2 predicted absolute LRS_i. The results suggest that P2 was most closely linked to LRS_i in the wild‐type population studied, a finding which may be common to species with strong second male sperm precedence. The study illustrates how P1 and P2 can have differing relationships with a male's overall reproductive success, and highlights the importance of understanding commonly used measures of sperm competition in the currency of fitness.     

PRONOUNCED WITHIN‐INDIVIDUAL PLASTICITY IN SPERM MORPHOMETRY ACROSS SOCIAL ENVIRONMENTS

Sperm morphometry (i.e., size and shape) and function are important determinants of male reproductive success and are thought to be under stabilizing selection. However, recent studies suggest that sperm morphometry can be a phenotypically plastic trait, which can be adjusted to varying conditions. We tested whether different behavioral strategies in aggression between aggressive red and nonaggressive black males of the color polymorphic Gouldian finch (Erythrura gouldiae) can influence sperm morphometry. We show pronounced within‐individual phenotypic plasticity in sperm morphometry of male Gouldian finches in three different social environments. Both red and black males placed in intermediate to high competitive environments (high frequency of red males) increased the relative length of their sperm midpiece. By contrast, red males placed in low to intermediate competitive environments (higher frequency of black males) increased the length of the sperm flagellum. Significant changes in stress and sex steroid hormone levels (in response to the competitive environment) appear to influence sperm traits in red but not in black males, suggesting that changes in hormonal levels are not solely responsible for the observed changes in sperm morphometry. These findings imply that males can adjust sperm morphometry across social environments.     

SPERM COMPETITION PROMOTES ASYMMETRIES IN REPRODUCTIVE BARRIERS BETWEEN CLOSELY RELATED SPECIES

Reproductive barriers between closely related species are often incomplete and asymmetric, but the evolutionary significance of these well-known phenomena remains unsolved. We test the hypothesis that the degree of gametic incompatibility in reciprocal crosses is associated to levels of sperm competition because this selective force favors both increased sperm competitiveness and ovum defensiveness. Using three species of Mus with high, intermediate, and low levels of sperm competition, we examined fertilization rates in competitive and noncompetitive contexts. We found that the influence of sperm competition upon sperm competitiveness is as strong as it is upon ovum defensiveness, revealing an effect upon female gametes so far overlooked. As a result, fertilization success was strongly related to differences in sperm competition levels between species providing sperm and ova, thus generating major asymmetries in reciprocal crosses. When placed in competition, conspecific sperm maintained levels of fertilization success similar to those found in noncompetitive contexts, at the expense of the success of heterospecific sperm. When only heterospecific sperm competed, species with highest levels of sperm competition outcompeted others and asymmetries were exacerbated. We conclude that sperm competition explains both the degree of gametic isolation and the degree of asymmetries between closely related species.     

SPERM DISPLACEMENT WITHOUT SPERM TRANSFER IN DROSOPHILA MELANOGASTER

In this paper we show that when Drosophila melanogaster females are mated twice, the semen of the second male causes a reduction of the effective number of resident sperm from the previous mating. This is demonstrated by two different kinds of experiments. In one set of experiments, mated females were remated to two different kinds of sterile males, one with normal semen and the other with deficient semen. The effect on the resident sperm was determined from the number of remaining progeny after mating to the sterile male, with the result that the normal semen reduced the amount of resident sperm in comparison with matings to the males with deficient semen. The second set of experiments employed interrupted matings. These experiments were based on the observation that semen is delivered before sperm during the first 5 min of copulation. The second matings were interrupted instantly, 2 min, and 4 min after the initiation of copulation. Compared to the instant interruptions, the two later interruptions had the effect of reducing the amount of resident sperm. The results of these two experiments clearly indicate that a sperm-incapacitation process plays a role in the well-documented phenomenon of sperm displacement (last-male advantage) in this species. Such a process could play a role in sperm displacement in the many cases where the mechanism is unknown.     

THE EVOLUTION OF SPERM SIZE IN BIRDS

Sperm size varies enormously among species, but the reasons for this variation remain obscure. Since it has been suggested that swimming velocity increases with sperm length, earlier studies proposed longer (and therefore faster) sperm are advantageous under conditions of intense sperm competition. Nonetheless, previous work has been equivocal, perhaps because the intensity of sperm competition was measured indirectly. DNA profiling now provides a more direct measure of the number of offspring sired by extrapair males, and thus a more direct method of assessing the potential for sperm competition. Using a sample of 21 species of passerine birds for which DNA profiling data were available, we found a positive relation between sperm length and the degree of extrapair paternity. A path analysis, however, revealed that this relationship arises only indirectly through the positive relationship between the rate of extrapair paternity and length of sperm storage tubules (SSTs) in the female. As sperm length is correlated positively with SST length, an increase in the intensity of sperm competition leads to an increase in sperm length only through its effect on SST length. Why females vary SST length with the intensity of sperm competition is not clear, but one possibility is that it increases female control over how sperm are used in fertilization. Males, in turn, may respond on an evolutionary time scale to changes in SST size by increasing sperm length to prevent displacement from rival sperm. Previous theoretical analyses predicting that sperm size should decrease as sperm competition becomes more intense were not supported by our findings. We suggest that future models of sperm-size evolution consider not only the role of sperm competition, but also how female control and manipulation of ejaculates after insemination selects for different sperm morphologies.     

BODY SIZE,SPERM COMPETITION,AND DETERMINANTS OF REPRODUCTIVE SUCCESS IN MALE SAVANNA BABOONS

One component of sexual selection is sperm competition. It has been reasoned that the intensity of sperm competition may be reflected in the relative testicular sizes of animals. Among males residing in multimale breeding systems, testicular size is relatively larger than among males residing in unimale mating systems. Information on whether differences in testicular size within a species can account for differences in male reproductive success is unavailable for natural populations of primates. A population of six troops of savanna baboons in Kenya was surveyed for morphometric analysis, and one of these troops was the subject of extensive behavioral observations afterwards. Testicular weights could not be obtained, but measurements of linear dimensions were transformed into volumetric estimates. Male weight accounted for 30% of the variance in testicular volume. Neither body size nor testicular volume was associated with differences in male reproductive activity. The outcome of fights over access to females could not be related to male body size, and ejaculatory patterns of males were independent of testicle size. Both sperm competition and aggressive competition intensified during the four-day optimum conception period, but fights over access to consort females were infrequent. Among savanna baboons, the probability of an ejaculation resulting in a conception is fairly low, which may account for the infrequency of injurious fights. Although testicle size influences sperm production, it does not influence either the timing of mating or the fertilizing capacity of spermatozoa, and both of these factors probably account for a substantial fraction of the variance in male baboon paternity. Sperm competition is an adjunct to agonistic competition as a mechanism affecting male baboon reproductive success. It is concluded that male reproductive success in baboons is affected more by social factors than by morphological traits associated with size.     

FEMALE CONTROL OF SPERM TRANSFER AND INTRASPECIFIC VARIATION IN SPERM PRECEDENCE: ANTECEDENTS TO THE EVOLUTION OF A COURTSHIP FOOD GIFT

Manipulation of ejaculates is believed to be an important avenue of female choice throughout the animal kingdom, but evidence of its importance to sexual selection remains scarce. In crickets, such manipulation is manifest in the premature removal of the externally attached spermatophore, which may afford females an important means of postcopulatory mate choice. We tested the hypothesis that premature spermatophore removal contributes significantly to intraspecific variation in sperm precedence by (1) experimentally manipulating spermatophore attachment durations of competing male Gryllodes sigillatus and (2) employing protein electrophoresis to determine the paternity of doubly mated females. The relative spermatophore attachment durations of competing males had a significant influence on male paternity, but the pattern of sperm precedence deviated significantly from the predictions of an ideal lottery. Instead, paternity data and morphological evidence accorded best with a model of partial sperm displacement derived here. Our model is similar to a displacement model of Parker et al. in that sperm of the second male mixes instantaneously with that of the first throughout the displacement process, but the novel feature of our model is that the number of sperm displaced is only a fraction of the number of sperm transferred by the second male. Regardless of the underlying mechanism, female G. sigillatus can clearly alter the paternity of their offspring through their spermatophore-removal behavior, and employ such cryptic choice in favoring larger males and those providing larger courtship food gifts. We discuss how female control of sperm transfer and intraspecific variation in sperm precedence may be important precursors to the evolution of gift giving in insects.     

COMPARATIVE EVIDENCE FOR THE EVOLUTION OF SPERM SWIMMING SPEED BY SPERM COMPETITION AND FEMALE SPERM STORAGE DURATION IN PASSERINE BIRDS

Sperm swimming speed is an important determinant of male fertility and sperm competitiveness. Despite its fundamental biological importance, the underlying evolutionary processes affecting this male reproductive trait are poorly understood. Using a comparative approach in a phylogenetic framework, we tested the predictions that sperm swim faster with (1) increased risk of sperm competition, (2) shorter duration of female sperm storage, and (3) increased sperm length. We recorded sperm swimming speed in 42 North American and European free-living passerine bird species, representing 35 genera and 16 families. We found that sperm swimming speed was positively related to the frequency of extrapair paternity (a proxy for the risk of sperm competition) and negatively associated with clutch size (a proxy for the duration of female sperm storage). Sperm swimming speed was unrelated to sperm length, although sperm length also increased with the frequency of extrapair paternity. These results suggest that sperm swimming speed and sperm length are not closely associated traits and evolve independently in response to sperm competition in passerine birds. Our findings emphasize the significance of both sperm competition and female sperm storage duration as evolutionary forces driving sperm swimming speed.     

EXPERIMENTAL EVOLUTION OF SPERM QUALITY VIA POSTCOPULATORY SEXUAL SELECTION IN HOUSE MICE

Individuals of many species copulate with multiple mates (polygamy). Multiple mating by females (polyandry) promotes sperm competition, which has broad implications for the evolution of the ejaculate. Multigenerational studies of polygamous insects have shown that the removal of sexual selection has profound fitness consequences for females, and can lead to an evolutionary divergence in ejaculate traits. However, the evolutionary implications of polygamous mating across successive generations have not before been demonstrated in a vertebrate. By manipulating the mating system we were able to reinstate postcopulatory sexual selection in a house mouse population that had a long history of enforced monogamy. Following eight generations of selection, we performed sperm quality assays on males from both the polygamous and monogamous selection lines. We applied a principal component analysis to summarize the variation among 12 correlated sperm traits, and found that males evolving under sperm competition had significantly larger scores on the first axis of variation, reflecting greater numbers of epididymal sperm and increased sperm motility, compared to males from lines under relaxed selection. Moreover, we found a correlated response in the size of litters born to females in lines subject to sperm competition. Thus, we present significant evidence that sperm competition has profound fitness consequences for both male and female house mice.     

VARIATION IN INDIVIDUAL FLOWERING TIME AND REPRODUCTIVE SUCCESS OF AGALINIS STRICTIFOLIA (SCROPHULARIACEAE)

Field studies on two populations of Agalinis strictifolia were conducted over a 3-year period to investigate the relationship between flowering time of individuals and plant size, flowering duration, flower and fruit production, fruit predation, and growth rate. Seasonal patterns of pollinator visitation were compared with those of individual flowering time, flower density, percent fruit production, and mean seeds/fruit. In general, early and middle flowering individuals (as determined by either first flowering date or peak flowering) were larger, flowered longer, and produced more flowers and fruits than late flowering individuals. Early and middle flowering individuals (based on first flowering date) also grew faster than late flowering individuals. Although early and middle flowering individuals produced more fruits, fruit predators did not damage a disproportionate number of fruits compared to late flowering individuals. Patterns of bee visitation showed no association with seasonal patterns of flower density, percent fruit production, mean seed/fruit, or individual flowering time. In populations of A. strictifolia, it would seem that biotic or environmental determinants of growth rate (hence size and reproductive success) may be more important in generating variation in individual flowering time than patterns of pollinator visitation or fruit predation.     

MATERNAL EFFECTS,BUT NO GOOD OR COMPATIBLE GENES FOR SPERM COMPETITIVENESS IN AUSTRALIAN CRICKETS

Explanations for the evolution of polyandry often center on the idea that females garner genetic benefits for their offspring by mating multiply. Furthermore, postcopulatory processes are thought to be fundamental to enabling polyandrous females to screen for genetic quality. Much attention has focused on the potential for polyandrous females to accrue such benefits via a sexy‐ or good‐sperm mechanism, whereby additive variation exists among males in sperm competitiveness. Likewise, attention has focused on an alternative model, in which offspring quality (in this context, the sperm competitiveness of sons) hinges on an interaction between parental haplotypes (genetic compatibility). Sperm competitiveness that is contingent on parental compatibility will exhibit nonadditive genetic variation. We tested these models in the Australian cricket, Teleogryllus oceanicus, using a design that allowed us to partition additive, nonadditive genetic, and parental variance for sperm competitiveness. We found an absence of additive and nonadditive genetic variance in this species, challenging the direct relevance of either model to the evolution of sperm competitiveness in particular, and polyandry in general. Instead, we found maternal effects that were possibly sex‐linked or cytoplasmically linked. We also found effects of focal male age on sperm competitiveness, with small increments in age conferring more competitive sperm.     

AN ASSESSMENT OF CHANGES WITH TIME IN THE MARKING PATTERNS USED FOR PHOTOIDENTIFICATION OF INDIVIDUAL SPERM WHALES, PHYSETER MACROCEPHALUS

We observed changes with time in the patterns of characteristic fluke markings used to identify sperm whales. Changes were categorized as minor, moderate, or major based on their severity. These change types were found to occur at rates of 0.9%, 11.8%, and 1.3% per individual per year, respectively. Gain and loss rates for each of seven different mark types were also calculated. The highest estimated rate was the gain of small nicks at 0.08 per individual per year. Most individuals identified by us possess at least a few characteristic marks and, therefore, changes of the type observed in this study are unlikely to severely affect their recognizability. For all but one mark type, gain rates were higher than loss rates, indicating that individuals may be accumulating marks with age. Over long periods this could eventually make individuals unrecognizable, with the result that population sizes calculated from these data may be overestimated. As long as photoidentification studies are conducted sufficiently often, and these changes are as gradual as they appear to be, this problem should be minimal.     

THE MAINTENANCE OF SPERM VARIABILITY: CONTEXT‐DEPENDENT SELECTION ON SPERM MORPHOLOGY IN A BROADCAST SPAWNING INVERTEBRATE

Why are sperm so variable despite having a singular, critical function and an intimate relationship with fitness? A key to understanding the evolution of sperm morphology is identifying which traits enable sperm to be successful fertilizers. Several sperm traits (e.g., tail length, overall size) are implicated in sperm performance, but the benefits of these traits are likely to be highly context dependent. Here, we examined phenotypic selection on sperm morphology of a broadcast spawning tube worm (Galeolaria gemineoa). We conducted laboratory experiments to measure the relationship between average sperm morphology and relative fertilization success across a range of sperm environments that were designed to approximate the range of sperm concentrations and ages encountered by eggs in nature. We found that the strength and form of multivariate selection varied substantially across our environmental gradients. Sperm with long tails and small heads were favored in high‐concentration environments, whereas sperm with long heads were favored at low concentrations and old ages. We suggest variation in the local fertilization environment and resulting differences in selection can preserve variability in sperm morphology both within and among males.     

POLLEN-TUBE COMPETITION,SIRING SUCCESS,AND CONSISTENT ASYMMETRIC HYBRIDIZATION IN LOUISIANA IRISES

Postpollination mechanisms can play an important role in limiting natural hybridization in plants. Reciprocal hand pollination experiments were performed to study these mechanisms in two species of Louisiana iris: Iris brevicaulis and I. fulva. Relative pollen-tube growth rates changed significantly through time, with I. fulva tubes increasingly outperforming I. brevicaulis tubes in both conspecific and heterospecific styles. However, this pattern of change in relative performance was a poor predictor of siring success: the majority of seeds sired by both maternal species was conspecific rather than hybrid. Experimental crosses and field studies show consistent asymmetric hybridization in Louisiana irises, with I. fulva being a more successful father and a more selective mother than both I. brevicaulis and a third species, I. hexagona. The cause of this pattern is not yet clear, but the pattern itself is unusual. Typically, short-styled species tend to be less successful in reciprocal crosses than long-styled relatives, but I. fulva has shorter styles than either I. brevicaulis or I. hexagona. The effects of pollen-tube competition, differential fertilization, and selective abortion in causing this pattern of asymmetric hybridization is discussed.