Natural and Sexual Selection in a Wild Insect Population R. Rodríguez-Muñoz, 1 A. Bretman, 1,2 J. Slate, 3 C. A. Walling, 4 T. Tregenza 1 * The understanding of natural and sexual selection requires both field and laboratory studies to exploit the advantages and avoid the disadvantages of each approach. However, studies have tended to be polarized among the types of organisms studied, with vertebrates studied in the field and invertebrates in the lab. We used video monitoring combined with DNA profiling of all of the members of a wild population of field crickets across two generations to capture the factors predicting the reproductive success of males and females. The factors that predict a male’s success in gaining mates differ from those that predict how many offspring he has. We confirm the fundamental prediction that males vary more in their reproductive success than females, and we find that females as well as males leave more offspring when they mate with more partners. I nsects are of fundamental importance to ter- restrial ecosystems but are underrepresented in studies that aim to understand how natural and sexual selection drive evolution in wild pop- ulations. Although poorly understood in their natural habitats, crickets have become an impor- tant laboratory model system, revealing complex forms of sexual selection whereby females choose between males according to their songs (1), males fight (2), females manipulate sperm from several males to favor unrelated males (3, 4), and females lay eggs faster when mated to dominant males (2). However, although we now have many insights into the behavior and physiology of crickets in the laboratory, we have almost no idea how important these various aspects are in the insects’ natural habitat. This discrepancy is a cause for concern: Laboratory situations remove some sources of selection that may be very important in wild pop- ulations and may create new pressures; for in- stance, it may be that males that sing more get more mates in the lab, but in the field such males may die younger. Univoltine flightless field crickets, Gryllus campestris, hatch from eggs in early summer. Nymphs build burrows among the grass and spend the winter underground, emerging in spring to undergo one or two final molts to adulthood. Both sexes are highly territorial and spend the vast majority of their time in the immediate vicinity of a burrow entrance. A few days after becoming adults, males start to sing, and both males and females start moving frequently from one burrow to another in search of mates. To identify selec- tive pressures affecting behavior and to observe how behavior is correlated with fitness, we built a network of 64 motion-sensitive, infrared-equipped video cameras allowing us to monitor occupied burrows 24 hours a day throughout the breeding season. We tagged every newly emerged adult with a unique code to analyze their lives and be- haviors, including mating partners, how long par- ticular males and females spent together, the time that each male spent singing calling songs to at- tract females, and the fights that almost invariably occur when a male approaches a burrow occu- pied by another male. We used these fights to score males as either dominant or subordinate, reflect- ing the proportion of fights that he won (5). Al- though females never share burrows, they are only very rarely involved in aggressive interac- tions. Females visit or receive visits from neigh- boring males and frequently remain with a male for hours or days, sharing his burrow and mating repeatedly. From our videos, we inferred adult life span as the time from the observed emer- gence to the point when a cricket was either seen to be killed by a predator or was no longer found at any burrow. We observed that females began mating a few days after becoming adults and laid eggs directly into the ground throughout the breeding season (burrows are narrow, so molting and mating take place just outside and are easily observed). The crickets in the field in the second year of our ob- servations are therefore the offspring of the adults from the previous summer. Populations may ex- perience some migration, but this is likely to be very limited in our study population. The mead- ow is relatively isolated, being surrounded by little suitable habitat, and the observed immigra- tion rates of adults are low; therefore we had high success in assigning parentage within the popu- lation (5). All of these factors indicate that it is unlikely that substantial numbers of adult off- spring were missed because of emigration. Life- time reproductive success (LRS) was therefore inferred from the assignment of parentage from parents in 2006 to offspring in 2007 through the genotyping of all adults at 11 microsatellite loci. A key prediction of the theory of sexual se- lection (6–8), assuming conventional sex roles and an even sex ratio, posits that males should have greater variance in LRS than females do. This prediction has been supported in a small number of studies of wild vertebrates [for exam- ple, (9)] and in laboratory experiments [although the lack of ecological context has led to debates over their relevance (10)]. Most studies of the cost and benefits of mates and matings in insects have been performed in the laboratory (11–13), and the only examination in the wild was of re- productive success estimated via the time female damselflies spent laying eggs after mating to a particular male (14). We directly examined both the number of mates that each individual had (controlling for differences in observational ef- fort) and the number of descendants they left in the next generation. The sex ratio was very close to even, which constrained the means to be the same for both sexes. As expected, we found that mean numbers of mates per day [males = 0.27 (0.40 SD), females = 0.25 (0.32 SD)] and of offspring sur- viving to adulthood [males = 1.92 (3.66 SD), fe- males = 1.79 (2.46 SD)] were, respectively, very similar. The small differences we observed were attributed to imperfections in observational data and in parentage assignment. The opportunity for selection can be estimated by comparing variances or coefficients of varia- tion (15). We examined with a randomization- 1 Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn TR10 EZ, UK. 2 School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK. 3 Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK. 4 Institute of Evolutionary Biology, School of Bi- ological Sciences, Ashworth Laboratories, King's Buildings, University of Edinburgh, Edinburgh EH9 3JT, UK. *To whom correspondence should be addressed. E-mail: t.tregenza@exeter.ac.uk Fig. 1. Number of adult offspring per individual. Frequencies for (A) females and (B) males. Males have significantly greater variance in offspring number relative to females. www.sciencemag.org SCIENCE VOL 328 4 JUNE 2010 1269 REPORTS on June 4, 2010 www.sciencemag.org Downloaded from