Sperm competition in Callosobruchus maculatus (Coleoptera: Bruchidae): a comparison of two methods used to estimate paternity

Abstract.

• 1 This study investigates sperm competition in Cullosobruchus maculatus (F.) (Coleoptera: Bruchidae), and is the first study to make a direct, controlled comparison of the sterile male and genetic marker techniques to estimate sperm precedence.
• 2 P₂ values (the proportion of offspring fathered by the second male) obtained from the two methods were similar: P₂ (sterile male) = 0.82, P₂ (genetic marker) = 0.85. Both methods are therefore suitable for studying sperm precedence if the appropriate correction factors are applied.
• 3 The importance of general fertilization ability, differential fertilizing capacity and differential zygote mortality are examined and discussed.

     

INDIVIDUAL VARIATION IN SPERM COMPETITION SUCCESS OF YELLOW DUNG FLIES,SCATOPHAGA STERCORARIA

Intraspecific variation in the proportion of offspring sired by the second male to mate with a female (P₂) is an aspect of sperm competition that has received little attention. We examined variation in the sperm competition success of individual male dung flies, Scatophaga stercoraria. In unmanipulated matings, copula duration was dependent on male size with smaller males copulating for longer. A principal component analysis was used to generate uncorrelated scores based on a male's size and copula duration. Using these scores demonstrated that P₂ values were dependent both on the relative size and copula durations of competing males. When copula duration was held constant, the success of an individual male increased as his body size, relative to the first male, increased. We interrupted copulations of “large” and “small” second males and fitted the resultant P₂ values to a linear model of sperm competition with unequal ejaculates. The data fit well to a model of sperm displacement in which sperm mix quickly on introduction to the sperm stores. Furthermore, they show that “large” males have a greater rate of sperm displacement than “small” males. The levels of prey availability during testis maturation may influence a male's success in sperm competition although his immediate mating history does not. We show why an understanding of variation in sperm competition success is important for understanding the mechanisms and evolutionary significance of sperm competition.     

Ejaculate traits in relation to male body size in the eastern mosquitofish Gambusia holbrooki

In the present study, the correlation between sperm number, sperm quality (speed, viability, longevity and length), sperm bundles quality (size and dissolving rate) and male body size has been tested in the eastern mosquitofish Gambusia holbrooki a poecilid species characterized by coercive mating tactics where males do not possess obvious ornaments, and the body size is the key determinant of pre‐copulatory male mating success. The results do not tally with theoretical predictions. Indeed, no correlation between male body size and either sperm or sperm‐bundle traits has been found, evidencing the lack of the theoretically expected trade‐off between the investment in characters involved in mate acquisition and the investment in ejaculate quality. An explanation for the observed pattern comes from the extremely dynamic mating system of G. holbrooki, characterized by variable size‐related male mating success and strong post‐copulatory selective pressure, with all males facing a similar high level of sperm competition. In this situation, a higher investment in growth and maintenance at the expense of ejaculate quality is not expected. These results underscore the necessity to comprehend detailed information on species’ reproductive biology and reproductive environment to understand both the evolution of ejaculate characteristics and possible deviations from theoretical predictions.     

Low Numbers of Sperm Retained in the Spermatheca May Explain the High Values of Sperm Precedence in the Migratory Locust, Locusta migratoria (Latr.)

Four hypotheses about the temporal variation of the number of spermatozoa in the spermatheca of once-mated females were tested in the migratory locust, Locusta migratoria. The best fit provided a regression model that assumed a sudden drop in sperm numbers being indicative of sperm ejection by females. Thereafter, one-fifth of an average ejaculate is stored. Low numbers of sperm stored do not lead to female sperm limitation, as none of the fitness parameters measured, fertilization success, hatching success, and offspring sex ratio, were correlated with the number of sperm present. Fertilization success decreased with successive egg pods. The offspring sex ratio was slightly male biased and tended to increase throughout the laying period. By applying our sperm ejection model to an independent data set of Parker and Smith (1975), we show that the low numbers of sperm retained by the female and subsequent sperm mixing rather than direct replacement may explain the high P₂ values found in this species.     

Sperm (ejaculate) competition in Drosophila melanogaster, and the reproductive value of females to males in relation to female age and mating status

• 1 In double mating experiments with Drosophila melanogaster in which one male had been irradiated, it was confirmed that sperm displacement is extensive, i.e. the second male to mate displaces most of the previously-stored sperm.
• 2 The predominance of the second ejaculate over the first increases with the interval between the two matings, from about P₂= 0.83 (second mating on the first day after the first mating) to about P₂= 0.99 (interval between mating = 14 days) where P₂ is the proportion of offspring fathered by the second male.
• 3 A more accurate method for calculating P₂ values is developed for experiments in which sperm are ‘labelled’ by irradiation treatment (equation 1).
• 4 Observations of the reducing egg production of the female throughout life were also obtained. A model is examined which incorporates both the sperm competition and egg production data to predict the reproductive value to a male of a mating with a given type of female, varying in age and mating status. The relative value (in terms of probable numbers of progeny gained) of a mating with a virgin or 4 day post-mating female is about twice that of a 14 day post-mating female, mainly because of the fecundity difference.
• 5 Some evolutionary aspects of sperm competition and multiple mating in insects are reviewed and discussed.

     

Adaptive control of copulation duration by males under sperm competition in the mite,Macrocheles muscaedomesticae

In a manure-inhabiting predatory mite, Macrocheles muscaedomesticae (Gamasida, Macrochelidae), when the female mates with two males, the first male takes nearly perfect fertilization priority (Yasui, 1988). The present study examined whether the first-male's sperm precedence is influenced by the copula-duration of the first and second males mating with the same female, and whether males control their copulation duration by assessing the probability that the mate has been inseminated by other males. Results of the artificial interruption of copulation showed that sperm precedence value, P₂ (the proportion of the offspring fathered by the second male), was negatively correlated with the copulation duration of the first male but positively correlated with that of the second male. There was a threshold (ca. 180–300 seconds) in the first-male's copulation duration beyond which P₂ decreased drastically; when length of the first copulation exceeded this threshold, the second males did not fertilize eggs, whereas they fertilized more than half of the eggs when the first-copulation duration was shorter than the threshold. Almost all males copulated for a longer period (average 509.8 seconds) than this threshold if the copulation duration of the previous male had not exceeded the threshold, but if it was longer than the threshold, second males had shortened their copulation (67.6 seconds). These results suggest that males are able to assess the insemination status of their mates and to adjust their copulation duration depending on the probability of fertilizing eggs by their own sperm. A mechanistic explanation for sperm precedence (i.e., plug-formation within sperm receptive organ of the females) is proposed.     

Environmental osmolality influences sperm motility activation in an anuran amphibian

Evolutionary theory predicts that selection will favour sperm traits that maximize fertilization success in local fertilization environments. In externally fertilizing species, osmolality of the fertilization medium is known to play a critical role in activating sperm motility, but there remains limited evidence for adaptive responses to local osmotic environments. In this study, we used a split‐sample experimental design and computer‐assisted sperm analysis to (i) determine the optimal medium osmolality for sperm activation (% sperm motility and sperm velocity) in male common eastern froglets (Crinia signifera), (ii) test for among‐population variation in percentage sperm motility and sperm velocity at various activation‐medium osmolalities and (iii) test for among‐population covariation between sperm performance and environmental osmolality. Frogs were obtained from nine populations that differed in environmental osmolality, and sperm samples of males from different populations were subjected to a range of activation‐medium osmolalities. Percentage sperm motility was optimal between 10 and 50 mOsm kg^?1, and sperm velocity was optimal between 10 and 100 mOsm kg^?1, indicating that C. signifera has evolved sperm that can function across a broad range of osmolalities. As predicted, there was significant among‐population variation in sperm performance. Furthermore, there was a significant interaction between activation‐medium osmolality and environmental osmolality, indicating that frogs from populations with higher environmental osmolality produced sperm that performed better at higher osmolalities in vitro. This finding may reflect phenotypic plasticity in sperm functioning, or genetic divergence resulting from spatial variation in the strength of directional selection. Both of these explanations are consistent with evolutionary theory, providing some of the first empirical evidence that local osmotic environments can favour adaptive sperm motility responses in species that use an external mode of fertilization.     

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.