PATERNITY IN EUSOCIAL HYMENOPTERA

Variation in paternity frequency in colonies of eusocial insects has p rofound effects on the relatedness among offspring and on the genetic diversity of colonies. Data on queen 'mating-frequency' in eusocial Hy menoptera vary in both quality and the phase of the 'mating' process t hey address. Some are observational studies of the range or maximum nu mber of copulations; others are derived from estimates of the number o f sperm in males and queens; others use genetic techniques to determin e the paternity of different males among female offspring. Only the la tter data can be used to calculate relatedness among offspring females . Previous reviews drew attention to these problems, but their results have established the impression that high paternity frequencies are c ommon, largely because multiple copulations are frequently observed. F or ants, we show that: (i) the range of observed copulations overestim ates effective paternity frequency; and (ii) the mean effective patern ity frequency in 19 species, for which accurate data based on allozyme analysis of mother - offspring combinations are available, is only 1. 16 (range 1-1.48). Over one third of these species have queens in whic h only one male contributes to paternity. Data from 34 species, which include less detailed genetic studies and four species studied using s perm counts, give similar results. Only two species, both Atta leaf cu tter ants and both studied using data on sperm stored in queen spermat hecas, appear to have effective insemination frequencies above two. Da ta on bees and wasps show a similar trend, We conclude that reliably d ocumented high paternity or insemination frequencies (> 2) are current ly restricted to one phylogenetically isolated and highly eusocial tax on each in ants, eusocial bees and wasps (Atta, Apis and Vespula, resp ectively). This pattern justifies the working hypothesis that multiple mating, by lowering the relatedness between female offspring and ther eby the benefits of reproductive helping behaviour, has not been a gen eral constraint for the evolution of eusociality in the Hymenoptera. U sing reliable data on paternity frequency and insemination, we re-anal yse two factors that it has been suggested correlate with mating frequ ency: colony population and number of egg-laying queens per colony. We find the following. 1. There is a significant positive correlation be tween paternity/insemination frequency and colony size for monogynous ants, but not for polygynous ants. This result seems to support the 's perm limitation' hypothesis, that queens which need to be highly fecun d copulate multiply to store sufficient sperm. We note, however, that the same trend is expected when large and/or long-lived colonies profi t more from having genetically diverse offspring. 2. There is no signi ficant negative correlation between paternity/insemination frequency a nd number of queens per colony. However, when the analysis is restrict ed to species with large colonies and no intranidal mating, the correl ation between paternity frequency and queen number becomes marginally significant. Several previous reviews have addressed the possible adap tive significance of multiple paternity. In contrast, and in keeping w ith the data that show single paternity to be frequent, we discuss sel ective reasons for single or low paternity. We compare the relative ef fects of multiple paternity and multiple maternity on genetic diversit y within colonies and show that they are not equivalent, and we also d iscuss directions for future research on paternity issues in social in sects.