Social Biology and Sex Ratios of the Eusocial Gall- Inducing Thrips Kladothrips Hamiltoni

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Social Biology and Sex Ratios of the Eusocial Gall- Inducing Thrips Kladothrips Hamiltoni L Ecological Entomology (1999) 24, 432±442 Social biology and sex ratios of the eusocial gall- inducing thrips Kladothrips hamiltoni BRENDA D. KRANZ, MICHAEL P. SCHWARZ, 1 2 LAURENCE A. MOUND andBERNARD J. CRESPI School of Biological Sciences, Flinders University, Australia, 1CSIRO Entomology, Canberra, Australia and 2Department of Biosciences, Simon Fraser University, Canada Abstract. 1. Thrips comprise the only order besides Hymenoptera where females are diploid and males are haploid. This makes them useful insects for studying the roles of kin selection and ecology in social evolution. 2. Kladothrips hamiltoni is one of six species of Australian gall-inducing thrips that have been identi®ed as eusocial. Galls are initiated by a single foundress, who rears her brood and remains within the enclosed gall for life. The adults of both sexes of her ®rst brood cohort are morphologically distinct from the second generation, comprising a nondispersing soldier caste. The foundress and sib-mated soldiers jointly produce a second, dispersing generation, approximately 60±80% of which are produced by the soldiers. Mean per capita egg production of female soldiers is less than 33% that of the foundress. 3. Adult eclosion of soldiers is protandrous but the overall sex ratio of the soldiers lacks bias (52% male). Protandry of soldiers increases the probability that female soldiers will be inseminated soon after their eclosion and therefore lay fertilised, female eggs. The lack of bias could be due to a balance between local resource competition and local mate competition. Gender-speci®c defensive behaviour of soldiers with their enemies may also be important in explaining this unexpected sex ratio. 4. The dispersing generation has an overall extreme female bias (5.6% male). Soldier incest increases relatedness between females more than between males, such that the foundress is more related to her granddaughters than her daughters, and female soldiers are more related to their daughters than their sons (assuming within-gall relatedness < 1). A female bias in the offspring of soldiers should be preferred by both the foundress and soldiers as they are more related to soldier- produced dispersing females than any other thrips in the gall. Female bias in the dispersing generation will also reduce local mate competition between males. Both soldier incest and local mate competition may therefore contribute to the extreme female bias in the dispersing generation. 5. Selection pressures for sociality in gall-inducing thrips appear to be more similar to those in gall-inducing aphids and naked mole rats than to those in Hymenoptera. Key words. Galls, haplodiploidy, incest, local mate competition, local resource competition, sex ratio, thrips. Correspondence: Brenda Kranz, School of Biological Sciences, Flinders University of South Australia, GPO Box 2100, Adelaide S.A. 5001, Australia. E-mail: brenda.kranz@¯inders.edu.au 432 # 1999 Blackwell Science Ltd R Sociality and sex ratio in a galling thrips 433 Introduction For these reasons, and because of the role that soldiers play in gall defence, Crespi(1992a,b) described Oncothrips tepperi Thysanoptera is the only order other than Hymenoptera where and O. habrus as eusocial, following the de®nition of Wilson all females are diploid and males are haploid (Stannard, 1968; (1971). Crespiand Mound (1997) further described Lewis, 1973; Crespi, 1991; Chapman & Crespi, 1998). This K. hamiltoni and other species with soldiers as eusocial, using makes thrips useful insects for studying the interplay between the de®nition of Crespi and Yanega (1995). haplodiploidy and kin selection in social evolution, because The aim of the study reported here was to examine the life- haplodiploidy has been postulated to be a key factor shaping history and social biology of K. hamiltoni in detail. Brood the evolution of sociality in Hymenoptera (Hamilton, 1964; development of the soldier and dispersing generations, Trivers & Hare, 1976). Kin selection theory predicts that for reproductive contributions of the foundress and soldiers to haplodiploid females, the genetic payoffs for altruism towards the dispersing brood, and the sex ratio of each generation were sisters are greater than for rearing daughters or sons, and lower investigated. The results are discussed in terms of kin selection still for helping to rear brothers, whereas males should and sex ratio biasing factors such as local mate competition concentrate on direct reproduction (Trivers & Hare, 1976); (Hamilton, 1967) and local resource competition (Clark, however, the payoffs for rearing siblings depend on sex 1978). allocation and the reproductive value of males and females (see reviews by Bourke & Franks, 1995; Crozier & Pamilo, 1996). Materials and methods Six species of tubuliferan thrips that induce galls on Australian Acacia have been identi®ed as eusocial (Crespi, Study organism 1992a; Crespi& Mound, 1997). These thripshave a morphologically distinct soldier caste (reduced wings, anten- Kladothrips hamiltoni adults are about 2 mm long and nae, and melanisation; enlarged forelegs) that ®ghts invaders. induce tubular galls about 30 mm long by approximately 3 mm Phylogenetic analyses suggest that eusociality in these thrips in diameter. They occur on Acacia cambagei, a tree that grows may have had two independent origins (Mound et al., 1996; along episodic waterways in the Lake Eyre Basin region of Crespi& Mound, 1997; Crespi et al., 1997, 1998). Gall- central Australia (Mound & Crespi, 1995; Mound et al., 1996). inducing thrips are of particular interest in assessing the roles The basic life-cycle of K. hamiltoni is described by Mound and of ecology and genetics in the evolution of social behaviour in Crespi (1995) and is summarised here. Galls are initiated by a haplodiploids because their life-cycle and ecology differ single macropterous female. Following closure of the gall, the markedly from many other social insects. For example, thrips foundress lays eggs that develop into micropterous adults, with do not forage or nurse their young as do eusocial enlarged forelegs and reduced cuticular melanisation (sol- Hymenoptera. This is because galls act as nutrient sinks so diers), that defend against invaders, particularly Koptothrips that, as long as thrips feed on the cell contents of the gall, a and lepidopteran larvae. The foundress dies some time supply of nutrients is ensured until gall or plant senescence following soldier eclosion into adults. Most female soldiers (Raman, 1987; Ananthakrishnan & Gopichandran, 1993). have some ovarian development and lay eggs following death There may be selective pressure for some individuals to of the foundress. These eggs develop into macropterous specialise in gall defence, however. Gall-inducing thrips are dispersing adults that become the foundresses and their mates prone to attack by kleptoparasites and other enemies; galls of the next generation of galls. form highly attractive food and shelter resources in the arid habitats where eusocial thrips occur (Crespi, 1992a,b; Crespi & Mound, 1997; Crespi et al., 1997). Study site and ®eld collections Thrips are unusual among galling insects because the adult foundress lays her eggs after being enclosed within the gall. Kladothrips hamiltoni galls were collected from A. camba- There are currently 21 described species of tubuliferan gall- gei at two sites along Arckaringa Creek (27°56¢S, 134°44¢E inducing thrips in the genera Oncothrips, Kladothrips, and and 28°6¢S, 135°5¢E), approximately 1100 km north of Onychothrips (Mound, 1971; Mound & Crespi, 1995; Mound Adelaide, South Australia, in the southern Lake Eyre Basin. et al., 1996; Crespi & Mound, 1997). Species with a soldier One site was adjacent to Arckaringa Creek Homestead and the caste belong to the genera Kladothrips and Oncothrips (Mound other was 40 km SE of this site, where Arckaringa Creek et al., 1996). In these species, galls are usually initiated by a crosses the Coober Pedy to Oodnadatta road. Arckaringa Creek single female and the ®rst brood consists only of soldiers. This is usually a dry creek bed but ¯oods on average every 2± brood is followed by a second, dispersing generation in which 3 years, usually in late spring or early summer (November to the adults are morphologically indistinguishable from the gall February). Temperatures in Oodnadatta, the closest weather foundress. These dispersing adults are probably produced by station to the sites, range from ± 2.2 to 50.7 °C, the median both the foundress and soldiers, although the relative monthly rainfall ranges from 2.0 to 9.9 mm, and the median contributions of foundresses and soldiers have not been annual rainfall is 64.7 mm (Commonwealth of Australia, quanti®ed. Female soldiers are inseminated and lay eggs, 1998). although their fecundity is lower than that of their mother Collections were made at the Arckaringa Homestead site (Crespi, 1992a; Mound & Crespi, 1995; Kranz et al., 1998). between 7 December 1995 and 14 May 1996 (Table 1), and # 1999 Blackwell Science Ltd, Ecological Entomology, 24, 432±442 L 434 Brenda D. Kranz et al. Table 1. Summary data for galls censused between December 1995 and May 1996. n is the number of galls censused. Live foundress is the proportion of galls whose foundress was alive out of all galls sampled. Brood size is the mean number of eggs, larvae, pupae, and adult soldiers. Other data are means with standard errors. Live Proportion male Proportion Date n foundress Eggs 1st instars 1st instars Soldiers male soldiers
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