Paternity in eusocial Hymenoptera

Abstract

Variation in paternity frequency in colonies of eusocial insects has profound effects on the relatedness among offspring and on the genetic diversity of colonies. Data on queen ‘mating-frequency’ in eusocial Hymenoptera vary in both quality and the phase of the ‘mating’ process they address. Some are observational studies of the range or maximum number of copulations; others are derived from estimates of the number of sperm in males and queens; others use genetic techniques to determine the paternity of different males among female offspring. Only the latter 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 common, largely because multiple copulations are frequently observed. For ants, we show that: (i) the range of observed copulations overestimates effective paternity frequency; and (ii) the mean effective paternity 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 which only one male contributes to paternity. Data from 34 species, which include less detailed genetic studies and four species studied using sperm counts, give similar results. Only two species, both Atta leaf cutter ants and both studied using data on sperm stored in queen spermathecas, appear to have effective insemination frequencies above two. Data on bees and wasps show a similar trend. We conclude that reliably documented high paternity or insemination frequencies (> 2) are currently restricted to one phylogenetically isolated and highly eusocial taxon each in ants, eusocial bees and wasps ( Atta, Apis and Vespula , respectively). This pattern justifies the working hypothesis that multiple mating, by lowering the relatedness between female offspring and thereby the benefits of reproductive helping behaviour, has not been a general constraint for the evolution of eusociality in the Hymenoptera. Using reliable data on paternity frequency and insemination, we re-analyse two factors that it has been suggested correlate with mating frequency: colony population and number of egg-laying queens per colony. We find the following. 1. There is a significant positive correlation between paternity/insemination frequency and colony size for monogynous ants, but not for polygynous ants. This result seems to support the ‘sperm limitation’ hypothesis, that queens which need to be highly fecund copulate multiply to store sufficient sperm. We note, however, that the same trend is expected when large and/or long-lived colonies profit more from having genetically diverse offspring. 2. There is no significant negative correlation between paternity/insemination frequency and number of queens per colony. However, when the analysis is restricted to species with large colonies and no intranidal mating, the correlation between paternity frequency and queen number becomes marginally significant. Several previous reviews have addressed the possible adaptive significance of multiple paternity. In contrast, and in keeping with the data that show single paternity to be frequent, we discuss selective reasons for single or low paternity. We compare the relative effects of multiple paternity and multiple maternity on genetic diversity within colonies and show that they are not equivalent, and we also discuss directions for future research on paternity issues in social insects.

An Alpine ant’s behavioural polymorphism: monogyny with and without internest aggression inTetramorium alpestre

“…A non-detection error (NDE) for each nest was calculated following Boomsma and Ratnieks (1996). The NDE is the probability that two males share the same genotype at all loci by chance, which might cause underestimation of queen-mating frequencies.…”

Paternity skew in seven species of honeybees (Hymenoptera: Apidae: Apis)

“…First, patrilines could remain undetected because the queen's offspring by chance may show identical genotypes despite being sired by different drones. This "nondetection-error" (Boomsma and Ratnieks, 1996) depends on the number of polymorphic alleles of the genetic markers used to analyze the population Paternity skew in honeybees 203 samples. However, the resolution of the used microsatellite loci was generally high in all studies (high numbers of loci and alleles), resulting in similar nondetection errors for the different data sets in Table I.…”

Multiple mating and facultative polygyny in the Panamanian leafcutter ant Acromyrmex echinatior

“…The only shortcomings of this procedure were that multiple mating could not be detected if mates had identical genotypes (Pamilo 1982;Boomsma and Ratnieks 1996), and that some paternal genotypes remained uncertain when a heterozygous queen had diploid o spring with an identical heterozygous genotype (Pamilo 1982). In cases like this, mating frequencies of queens were estimated parsimoniously, so that when there was uncertainty about whether a colony had a heterozygous queen that had mated once, or a homozygous queen mated twice, the former was always assumed.…”

“…Hypotheses of the latter type fall into four general subcategories, where ®tness advantages to multiply mated queens accrue by (1) a genetically more diverse worker force with a more ecient division of labour (Crozier and Page 1985;Page and Robinson 1991), (2) a genetically more diverse worker force that is more resistant to infectious diseases (Hamilton 1987;Sherman et al 1988;Shyko and Schmid-Hempel 1991;Schmid-Hempel 1994), (3) reduced colony-level genetic load due to production of diploid (sterile) males (Crozier and Page 1985;Pamilo et al 1994), and (4) reduced worker-queen con¯ict over sex allocation ratio and male parentage (Starr 1984;Moritz 1985;Queller 1993;Moritz et al 1995;Ratnieks and Boomsma 1995). A considerable number of ant species have been reported to mate multiply, but most of these reports have been observations of multiple copulations, whereas documented cases of high e ective queen mating frequencies in ants are rare (see Boomsma and Ratnieks 1996 for a review). Ant species or populations where both polyandry and polygyny signi®cantly reduce relatedness among nestmate workers have so far only been reported in Formica (Pamilo 1993;SundstroÈ m 1993).…”

“…Multiple mating by queens may be an adaptive trait if singly mated queens risk eventual sperm depletion (Cole 1983;, or if colonies with genetically more diverse o spring have a selective advantage (recently reviewed by Boomsma and Ratnieks 1996). Hypotheses of the latter type fall into four general subcategories, where ®tness advantages to multiply mated queens accrue by (1) a genetically more diverse worker force with a more ecient division of labour (Crozier and Page 1985;Page and Robinson 1991), (2) a genetically more diverse worker force that is more resistant to infectious diseases (Hamilton 1987;Sherman et al 1988;Shyko and Schmid-Hempel 1991;Schmid-Hempel 1994), (3) reduced colony-level genetic load due to production of diploid (sterile) males (Crozier and Page 1985;Pamilo et al 1994), and (4) reduced worker-queen con¯ict over sex allocation ratio and male parentage (Starr 1984;Moritz 1985;Queller 1993;Moritz et al 1995;Ratnieks and Boomsma 1995).…”