Colonies on the march move maternal alleles across tropical landscapes

A blog post highlighting the article by Soare et al. in Insectes Sociaux.

By Sean O’Donnell

Army ants are strange beasts. New World army ants (Ecitoninae) share a suite of unusual characteristics, including mass foraging raid behavior, that distinguish them among ants and indeed among all social insects- the army ant syndrome. Their strangeness may breed success: recent evolutionary analyses suggest the army ant syndrome is ancient (perhaps 80 million years old), and army ants are among the most important ecological players in the tropical forests where they thrive.

One component of the army ant syndrome relates to their mode of reproduction. Like some other social insects, notably honeybees (Apis) and some paper wasps (Epiponini), army ant colonies reproduce by swarming. Swarming involves groups of workers and one or more reproductives (queens, in Hymenoptera) moving away from the natal colony to establish a new daughter colony. Army ants are unusual because their impressively large queens are wingless. During periodic bouts of reproduction that occur every few years, an army ant colony produces a single surviving daughter queen who mates with a number of visiting winged males that arrive from distant colonies. After mating, the young queen inherits about half of the worker force and walks away from her natal colony to start a new society.

Differences in mobility between queens and males occur in some ant species and are usually associated with significant sex differences in dispersal distance. In these species of dependent-founding ants, homebody queens settle in or near their natal nests; males fly longer distances to seek mates. This sex difference can be important for population structure: the mobile longer-flying males move genes (alleles) greater distances. It was long assumed that wingless army ant queens were relatively mobility-challenged, and that queens were therefore less important than winged army ant males for maintaining gene flow in army ant populations.

However, another unusual key feature of the army ant syndrome is colony nomadism. Army ants do not dig and occupy permanent nests. Rather, they regularly move or emigrate among a series of temporary shelters where they bivouac, assembling a temporary nest from the interlinked bodies of the workers. In the well-studied species Eciton burchellii, colonies are on a five-week cycle, of which two weeks are spent emigrating among a series of nesting sites. Single emigrations can traverse 100 m linear distance. Successive emigrations tend toward directionality: a right turn on one night’s emigration path is likely to be followed by a left turn the following night. Do such colony movements, summed over the three years between reproductive bouts, contribute to maternal (female) gene flow?

Video of an an Eciton burchellii colony starting to emigrate. Source: S. O’Donnell.

We hypothesized that colony emigrations would contribute to maternal gene flow and reduce or eliminate sex biases in gene dispersal. We tested for sex biases in gene flow by measuring the genetic relatedness among males and females (queens) in a population of the army ant Eciton burchellii parvispinum in the mountains of Costa Rica. We collected samples of workers from a total of 40 colonies in a roughly 10 km X 10 km area. We sampled colonies in the same geographic area in 2006 (25 colonies), and again roughly three years later in 2009 (15 colonies). Three years represents the typical generation time (time between reproductive bouts) for E. burchellii colonies.

We genotyped workers by using PCR primers to amplify seven highly variable microsatellite DNA regions. We then reconstructed the maternal (queen) genotype for each colony as well as the genotypes of the males that had fathered the workers we sampled. We asked whether relatedness among the queens and their mates decreased with distance among the colonies with years, as well as testing for spatial genetic structure between the 2006 and 2009 samples.

We found no significant difference in spatial genetic structure between the sexes, either within or between the 2006 and 2009 samples. In fact, there was some evidence against genetic philopatry for queens: the queens sampled in 2009 were significantly unrelated to queens sampled in 2006 that were collected nearby (within 0.5 km). These patterns suggest maternal dispersal via emigrations contributed to gene flow in these army ants, reducing or eliminating male biases in dispersal. Because colony emigrations summed over the lifetime of army ant queens queen may contribute to gene flow across the landscape. The ecological consequences mean that habitat connectivity is essential to permit colony emigrations and support genetic diversity in populations of this keystone species.

 

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