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Larval Helpers and Age Polyethism in Ambrosia Beetles

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Larval Helpers and Age Polyethism in Ambrosia Beetles Larval helpers and age polyethism in ambrosia beetles Peter H. W. Biedermann1 and Michael Taborsky Department of Behavioral Ecology, Institute of Ecology and Evolution, University of Bern, CH-3012 Bern, Switzerland Edited by Bert Hölldobler, Arizona State University, Tempe, AZ, and approved September 1, 2011 (received for review May 14, 2011) Division of labor among the workers of insect societies is a the role of division of labor is unknown. Ambrosia beetles live conspicuous feature of their biology. Social tasks are commonly inside trees, which is a habitat extraordinarily favoring social shared among age groups but not between larvae and adults with evolution (12), apparently having fostered at least seven in- completely different morphologies, as in bees, wasps, ants, and dependent origins of fungiculture in beetles (13). Hence, they beetles (i.e., Holometabola). A unique yet hardly studied holome- represent a unique model system to study the evolution of so- tabolous group of insects is the ambrosia beetles. Along with ciality in relation to fungiculture. Interestingly, ambrosia beetles one tribe of ants and one subfamily of termites, wood-dwelling vary in their mating system (inbreeding vs. outbreeding species) ambrosia beetles are the only insect lineage culturing fungi, a trait and ploidy level (haplodiploid vs. diploid species), which are predicted to favor cooperation and division of labor. Their sociality factors that have been assumed to contribute to social evolution, has not been fully demonstrated, because behavioral observations although their respective roles in social evolution are contro- have been missing. Here we present behavioral data and experi- versial (1). The ambrosia beetle subtribe Xyleborini is charac- ments from within nests of an ambrosia beetle, Xyleborinus sax- terized by regular inbreeding, haplodiploidy, and fungiculture (8, esenii. Larval and adult offspring of a single foundress cooperate 14). High relatedness and haplodiploidy in combination with an in brood care, gallery maintenance, and fungus gardening, show- extremely female-biased sex ratio are factors predisposing them ing a clear division of labor between larval and adult colony mem- to advanced sociality (1). Additionally, cooperation in fungi- bers. Larvae enlarge the gallery and participate in brood care and culture is likely because a single individual can hardly maintain gallery hygiene. The cooperative effort of adult females in the a fungus garden on its own (10). Indeed, it was shown that adult colony and the timing of their dispersal depend on the number female offspring delay dispersal from their natal gallery, which of sibling recipients (larvae and pupae), on the presence of the results in an overlap of eggs, larvae, pupae, and at least two mother, and on the number of adult workers. This suggests that generations of adult offspring within a colony (8). A helper effect altruistic help is triggered by demands of brood dependent on of philopatric females has been indicated by the fact that the care. Thus, ambrosia beetles are not only highly social but also number of staying females that do not reproduce correlates show a special form of division of labor that is unique among positively with gallery productivity in Xyleborinus saxesenii Rat- holometabolous insects. zeburg (8). Behavioral observations of ambrosia beetles within their galleries have been missing so far, however, because it is altruism | cooperative fungiculture | insect agriculture | larval workers | virtually impossible to observe them in nature inside the wood. mutualism The only report on eusociality in ambrosia beetles is not based on behavioral data, but reproductive roles have been inferred by ivision of labor enhances work efficiency and is fundamental destructive sampling of active nests of Austroplatypus incompertus to the biological evolution of social complexity (1). This (9). To facilitate observations of beetle behaviors inside galleries, D fi conspicuous feature of social insects largely explains their eco- we developed arti cial observation tubes to contain entire col- logical success (2). Task specialization in insects usually occurs onies of reproducing beetles (15, 16). Here we use this breeding between different age groups. Individuals either pass through technique of X. saxesenii to ask (i) whether offspring produced in consecutive molts during development (Hemimetabola; e.g., a gallery engage in alloparental brood care and fungus mainte- termites, aphids), with immatures resembling small adults and nance, (ii) whether different types of individuals specialize in divergent tasks, and (iii) whether decisions to help and to dis- division of labor occurring typically between such larval nymphs perse relate to the number of potential beneficiaries and the that may show morphological specializations [e.g., first-instar number of potential workers present in the colony. Furthermore, soldier aphids (3)]; or individuals metamorphose by dramatically we evaluate experimentally (iv) whether female dispersal depends reorganizing their morphology during the pupal stage (Hol- on the presence of an egg-laying foundress, because her removal ometabola; e.g., bees, wasps, ants, beetles), which predestines should affect the need for alloparental care. We compare our larvae and adults to specialize in different tasks because of their results with the patterns of sociality known from other major morphological and physiological differentiation. Indeed, larvae insect taxa. of the eusocial Hymenoptera, for example, may produce nest- building silk [weaver ants (4)] and may supply adults with extra Results enzymes and nutrients [trophallaxis in several wasps and ants (2, Age- and Sex-Specific Behavior. Gallery maintenance and brood care 5, 6)]. However, all known cooperative actions of holometabo- were allocated differently between different age classes within lous larvae are apparently completely under adult control (2), anest(Fig.1andTable S1). The gallery was extended mainly by and despite the potential for the evolution of highly specialized larvae (digging), which also reduces the spread of mold (SI Text immature helper morphs, larvae of these taxa are largely im- and Fig. S1), whereas fungus care (cropping) and brood protection mobile and helpless and in need of being moved, fed, and cared (blocking) were exclusively conducted by adults. Blocking was only for by adults (7). In ambrosia beetles, however, in which co- operative breeding (8) and eusociality (9) also have been as- sumed, larvae can move and forage independently in the nest, Author contributions: P.H.W.B. and M.T. designed research; P.H.W.B. performed research; which provides great potential for division of labor between P.H.W.B. analyzed data; and P.H.W.B. and M.T. wrote the paper. larvae and adults. The authors declare no conflict of interest. Division of labor sets the stage for the origin of fungiculture in This article is a PNAS Direct Submission. fungus-growing ants and termites (10). Ambrosia beetles origi- 1To whom correspondence should be addressed. E-mail: [email protected]. nate from solitary or colonial ancestors, and their fungus agri- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. culture may have coevolved with sociality (8, 10, 11). However, 1073/pnas.1107758108/-/DCSupplemental. 17064–17069 | PNAS | October 11, 2011 | vol. 108 | no. 41 www.pnas.org/cgi/doi/10.1073/pnas.1107758108 Downloaded by guest on September 30, 2021 EVOLUTION Fig. 1. Division of labor and age polyethism between age and sex classes in X. saxesenii. Bars show the mean (±SE) proportions of time larvae, teneral females, mature females, and males performed different cooperative tasks. Statistically significant differences between the classes are denoted by different letters (P < 0.05; GEE, details in Table S1). Note scale differences between A–C and D–F. performed by foundresses and mature females, and in 33 of 35 fungal layer on each other’s bodies by allogrooming. In males, cases only one individual blocked at a time. In the 25 cases (in 19 allogrooming was frequently followed by a mating attempt; it may of 93 galleries) when we did not observe a blocking female, the thus serve also to obtain information about female mating status. following behavioral scan revealed that larvae had crawled out of the gallery. At least 71 larvae (x = 3.7 larvae per gallery) died in Adult Female Behaviors Depending on Gallery Composition. The this manner, which suggests that an important function of blocking proportion of time adult females exhibited cropping and allog- is to prevent larvae from getting accidentally lost. rooming and the occurrence of blocking were higher during gal- Larvae and adults took different shares in hygienic behaviors. lery stages when brood dependent on care was present in the Only larvae compressed dispersed waste into compact balls colony (preadult and larval-adult gallery stages) than during other (balling; Movie S1). Frass-balls, pieces of wood, or parts of dead times (postlarval gallery stage; Table S2). Shuffling was shown siblings were moved within the gallery and pushed out of the equally often before, during, and after larval presence within entrance (shuffling; Movie S2) mainly by mature females but to a gallery, whereas adult female digging tended to increase per some extent also by larvae and teneral females (Fig. 1 and Table capita after pupation of the last larva. Cannibalism was not shown S1). The ultimate waste disposer was always the mature female before the hatching of adult daughters, and it occurred more that was blocking the entrance. Cannibalism was directed toward often when dependent offspring were still present. Dispersal of adult beetles (1 case), pupae (3 cases), and larvae (37 cases) that adult females seemed to be contingent on brood care demands: it were already dead (in most cases) or that did not respond to significantly increased in the 10 d after a major proportion of being groomed. In such cases the groomer (larva or adult) would larvae had completed their development relative to the 10 d be- use its mandibles to open the body of the groomed sibling within fore (Wilcoxon: z = −3, P < 0.001, n = 23; Fig.
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