Abstract
The unique nomadic life-history pattern of army ants (army ant adaptive syndrome), including obligate colony fission and strongly male-biased sex-ratios, makes army ants prone to heavily reduced effective population sizes (N e). Excessive multiple mating by queens (polyandry) has been suggested to compensate these negative effects by increasing genetic variance in colonies and populations. However, the combined effects and evolutionary consequences of polyandry and army ant life history on genetic colony and population structure have only been studied in a few selected species. Here we provide new genetic data on paternity frequencies, colony structure and paternity skew for the five Neotropical army ants Eciton mexicanum, E. vagans, Labidus coecus, L. praedator and Nomamyrmex esenbeckii; and compare those data among a total of nine army ant species (including literature data). The number of effective matings per queen ranged from about 6 up to 25 in our tested species, and we show that such extreme polyandry is in two ways highly adaptive. First, given the detected low intracolonial relatedness and population differentiation extreme polyandry may counteract inbreeding and low N e. Second, as indicated by a negative correlation of paternity frequency and paternity skew, queens maximize intracolonial genotypic variance by increasingly equalizing paternity shares with higher numbers of sires. Thus, extreme polyandry is not only an integral part of the army ant syndrome, but generally adaptive in social insects by improving genetic variance, even at the high end spectrum of mating frequencies.
Highlights
Army ants are major arthropod predators and important keystone organisms in tropical and subtropical ecosystems, with a strong impact on the population dynamics of their prey and species community structures [1,2,3,4,5]
Except for the E. mexicanum colony Em1, a single queen genotype explaining all worker genotypes could be inferred with 100% support in MATESOFT
The remaining two unassigned workers were excluded for having possibly originated from a second queen as it might occur after recent colony fission
Summary
Army ants are major arthropod predators and important keystone organisms in tropical and subtropical ecosystems, with a strong impact on the population dynamics of their prey and species community structures [1,2,3,4,5]. This is facilitated by a highly specialized combination of traits, the so called army ant adaptive syndrome, which includes group raiding and nomadism [6,7,8]. Several hypotheses have been put forward to explain the adaptive value of such high degrees of polyandry in social insects, mainly invoking the enhancement of genotypic variance within colonies, and the potential to increase overall Ne and counteract the risk of inbreeding
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