Worker Caste Determination in the Army Ant Eciton Burchellii

Biol. Lett. the worker collective can also be differentiated into doi:10.1098/rsbl.2007.0257 multiple castes as a result of differences in allometric Published online growth during larval development (Oster & Wilson Evolutionary biology 1978; Ho¨lldobler & Wilson 1990). Traditionally, environmental factors have been assumed to be the main drivers of caste differentiation (Oster & Wilson Worker caste 1978; Robinson 1992), but genetic effects on queen– worker caste determination are known for some bees determination in the army and ants (Kerr 1950; Julian et al. 2002; Volny & ant Eciton burchellii Gordon 2002; Moritz et al. 2005). Furthermore, genetic components in the determination of worker Rodolfo Jaffe´ 1,*,†, Daniel J. C. Kronauer2,†, polymorphism have been demonstrated in some ant F. Bernhard Kraus3, Jacobus J. Boomsma2 species, where queens are either inseminated by many and Robin F. A. Moritz1 males (polyandry) or where colonies are headed by 1Institut fu¨r Biologie, Martin-Luther-Universita¨t Halle-Wittenberg, several reproducing queens (polygyny). In these Hoher Weg 4, 06099 Halle/Saale, Germany cases, the workers of different families or subfamilies 2 Department of Population Biology, Institute of Biology, University of within a colony develop under very similar conditions, Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark 3El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo allowing for the detection of genetic effects on caste Aeropuerto km 2.5, C.P. 30700 Tapachula, Chiapas, Mexico differentiation. Two studies on polygynous ant species *Author for correspondence ([email protected]). have reported that worker size is influenced by the †These authors contributed equally to this work. genotypes of mother queens and their mates (Fraser Elaborate division of labour has contributed et al. 2000; Schwander et al. 2005). However, it is significantly to the ecological success of social difficult to exclude differences in rearing environment insects. Division of labour is achieved either by between the offspring of different queens as a con- behavioural task specialization or by morphological specialization of colony members. In founding factor in studies of polygynous species physical caste systems, the diet and rearing (Fraser et al. 2000). Two further studies on ant environment of developing larvae is known to species with polyandrous queens in single queen determine the phenotype of adult individuals, colonies have demonstrated a genetic effect on worker but recent studies have shown that genetic differentiation into either small or large workers components also contribute to the determina- (Hughes et al. 2003; Rheindt et al. 2005). However, a tion of worker caste. One of the most extreme species providing both extreme intracolonial genetic cases of worker caste differentiation occurs in variation via polyandry, and extreme morphological the army ant genus Eciton, where queens mate with many males and colonies are therefore worker polymorphism, would be the most suitable composed of numerous full-sister subfamilies. model to test the generality of genetic effects on caste This high intracolonial genetic diversity, in com- differentiation in insect societies. bination with the extreme caste polymorphism, Eciton burchellii, an army ant of New World tropical provides an excellent test system for studying forests, shows an extreme worker polymorphism with the extent to which caste determination is four recognized physical worker castes (Franks 1985; genetically controlled. Here we show that genetic figure 1). Moreover, E. burchellii queens typically effects contribute significantly to worker caste mate with 10–20 males, resulting in a large number fate in Eciton burchellii. We conclude that the combination of polyandry and genetic variation of worker patrilines (full-sib families with the same for caste determination may have facilitated the mother and father) in each colony (Kronauer et al. evolution of worker caste diversity in some 2006). Taking advantage of this combination of social lineages of social insects. traits, we show that genes have a significant effect on Keywords: division of labour; polyandry; worker caste determination. multiple mating; worker polymorphism; social insects 1. INTRODUCTION Division of labour increases efficiency and has contributed significantly to the ecological success of insect societies (Oster & Wilson 1978; Bourke & Franks 1995). Worker specialization in colonies requires behavioural or morphological differentiation among nest members, which can be achieved either by assuming temporary roles or by the evolution of permanently differentiated morphological castes (Oster & Wilson 1978). The most fundamental physical caste differentiation in social insects is the reproductive division of labour between workers and queens. However, in Figure 1. Extreme worker polymorphism of the army ant E. burchellii. Here, a major with ivory-coloured head and termites and approximately 15% of the ant genera, sabre-shaped mandibles guards a raiding column in which Electronic supplementary material is available at http://dx.doi.org/ smaller workers carry prey items (photograph by D. J. C. 10.1098/rsbl.2007.0257 or via http://www.journals.royalsoc.ac.uk. Kronauer). Received 11 May 2007 This journal is q 2007 The Royal Society Accepted 28 June 2007 2 R. Jaffe´ et al. Worker caste determination in army ants M1 8 23 M2.1 V1 3 9 12 20 14 14 7 13 17 10 12 16 6 * 11 24 17 10 * 31 14 4 18 9 27 2 5 ** 14 9 5 17 516 410 1 2 4 6 8 10 12 14 2 4 6 2 4 6 8 10 12 * 8 9 M3 26 6 M2.2 8 V2 3 16 8 8 8 9 7 14 19 23 72129 head width (mm) 30 17 4 14 4 16 18 ** 19 16 6 6 2 8 21 11 13 5 1 majors submajors medias minors 2 4 6 8 10 1224 68 2 4 6 8 10 12 patriline Figure 2. Ranked worker head width variation among the most frequent patrilines (865 genotyped workers) of five E. burchellii colonies (six matrilines). Caste size ranges are indicated by different grey shadings. Overall caste representation among patrilines was significantly skewed ( p!0.01). Significant biases in caste representation within individual patrilines are indicated by Ãp!0.05 and ÃÃp!0.01, while mean values, standard errors and standard deviations are represented by horizontal bars, grey boxes and whiskers, respectively. Sample sizes are given above the whiskers. 2. MATERIAL AND METHODS 3. RESULTS (a) Genotyping We found that queens had mated with 13–25 males We genotyped a total of 1143 workers from three E. burchellii (arithmetic meanGs.e.: 16.7G0.4), with an effective colonies collected near Tapachula, Chiapas, Mexico (M1: nZ264, M2: nZ209 and M3: nZ271), and two colonies collected in number of matings between 9.4 and 17.8 (harmonic Parque Nacional Henri Pittier, Venezuela (V1: nZ200 and V2: meanGs.e.: 11.6G0.2) confirming earlier estimates nZ199), for different combinations of seven polymorphic DNA (Kronauer et al. 2006). Overall caste representation microsatellites (Denny et al. 2004). DNA extractions were per- among patrilines was highly significantly skewed formed following a Chelex protocol and PCR products were run on 2 an ABI377 or a MegaBACE 1000 capillary sequencer. (c147Z193.77, pZ0.006) and several patrilines were significantly biased towards producing certain worker (b) Patriline assignment morphs (figure 2; electronic supplementary material). Workers were assigned to patrilines using the program MATESOFT This demonstrates a considerable genetic component v. 1.0 ( Moilanen et al. 2004), as described by Kronauer et al. (2006). The probability that two males could not be distinguished in our influencing caste determination. The variance com- analysis was very low (between 0.01 and 3.7!10K5; Boomsma & ponent estimation resulted in an index of head width Ratnieks 1996). Since colony M2 consisted of offspring from two heritability of h2Z0.15 (G0.01 s.e.; lower 95% confi- queens (presumably due to a recent colony fission event), workers Z were assigned to the deduced queens following the most parsimonious dence limit 0.13), providing further evidence for a explanation based on Mendelian inference (Kronauer et al. 2004). significant genetic component to caste determination. (c) Analyses Sample size corrected effective queen mating frequencies were 4. DISCUSSION calculated according to Nielsen et al. (2003), with standard errors As in other social Hymenoptera with a demonstrated from jackknifing over colonies. In order to quantify the phenotypic variability, we measured maximum head width in 991 individuals genetic component for caste determination (Fraser (all those with more than three successfully amplified loci, unambi- et al. 2000; Page & Erber 2002; Hughes et al. 2003; guously assigned into a patriline containing more than one Rheindt et al. 2005; Schwander et al. 2005; Hughes & individual). Repeating the measurements for 20 individuals (five Boomsma 2007), the genetic control in E. burchellii is per caste) and performing a linear regression, we showed that our head width measurements were highly repeatable (r 2Z0.99, plastic rather than hard-wired. Most males were able to p!0.001). We grouped individuals into four distinct castes sire daughters of all worker castes (figure 2; electronic following Franks (1985): minors (less than 1.16 mm); medias supplementary material) and the additive genetic (1.27–1.72 mm); submajors (1.84–2.51 mm); and majors (above variance accounted for only 15% of the total observed 2.63 mm). We employed a c2 analysis to test whether the distribution of worker castes deviated from homogeneity across polymorphism,

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