In polygamous systems, male fitness is determined not only by mating success but also by fertilization success. Despite the growing interest over the past several decades in postcopulatory sexual selection, its relative importance compared to precopulatory sexual selection remains a subject of debate. Here, we use extensive behavioral observations of a seminatural population of Hawaiian swordtail crickets, Laupala cerasina, and molecular paternity assignment to measure the opportunities for pre- and postcopulatory selection. Because postcopulatory selection has the potential to operate at multiple stages, we also separately attribute its effects to factors specific to mating events versus factors specific to males. We find that variance in postcopulatory success is over four times as great as variance in precopulatory success, with most of it unexplained by male mating order or the number of nuptial gifts given. Surprisingly, we also find that male singing effort is under postcopulatory selection, suggesting that males who sing more frequently also have more competitive ejaculates. Our results are consistent with the hypothesis that high polyandry levels promote greater relative postcopulatory selection. They also highlight the need for detailed behavioral observations under conditions as natural as possible when measuring mating and reproductive success.

When females mate multiply, postcopulatory sexual selection can occur via sperm competition and cryptic female choice. Although postcopulatory selection has the potential to be a major force in driving evolution, few studies have estimated its strength in natural populations. Likewise, although polyandry is widespread across taxa and is the focus of a growing body of research, estimates of natural female mating rates are still limited in number. Microsatellites can be used to estimate the number of mates represented in females' sperm stores and the number of sires contributing to their offspring, enabling comparisons both of polyandry and of two components of postcopulatory selection: the proportion of males that mate but fail to sire offspring, and the degree of paternity skew among the males that do sire offspring. Here, we estimate the number of mates and sires among wild females in the Hawaiian swordtail cricket Laupala cerasina. We compare these estimates to the actual mating rates and paternity shares we observed in a semi-natural population. Our results show that postcopulatory sexual selection operates strongly in this species: wild females mated with an average minimum of 3.6 males but used the sperm from only 58% of them. Furthermore, among the males that did sire offspring, paternity was significantly skewed. These patterns were similar to those observed in the field enclosure, where females mated with an average of 5.7 males and used the sperm from 62% of their mates, with paternity significantly skewed among the sires.

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Oxidative damage increases with age in a variety of cell types, including sperm, which are particularly susceptible to attack by reactive oxygen species (ROS). While mitochondrial respiration is the main source of cellular ROS, the relationship between the rates of aerobic metabolism and ROS production, and how this relationship may be affected by age, both in sperm and in other cell types, is unclear. Here, we investigate in Drosophila melanogaster sperm, the effects of male age on (i) the level of hydrogen peroxide in the mitochondria, using a transgenic H2O2 reporter line; (ii) the in situ rate of non-H2O2 ROS production, using a novel biophysical method; and (iii) metabolic rate, using fluorescent lifetime imaging microscopy. Sperm from older males had higher mitochondrial ROS levels and a higher metabolic rate but produced ROS at a lower rate. In comparison, a somatic tissue, the gut epithelium, also showed an age-related increase in mitochondrial ROS levels but a decrease in metabolic rate. These results support the idea of a tissue-specific optimal rate of aerobic respiration balancing the production and removal of ROS, with aging causing a shift away from this optimum and leading to increased ROS accumulation. Our findings also support the view that pathways of germline and somatic aging can be uncoupled, which may have implications for male infertility treatments.