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Inbreeding and Disease Resistance in a Social Insect: Effects of Heterozygosity on Immunocompetence in the Termite Zootermopsis Angusticollis Daniel V

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Inbreeding and Disease Resistance in a Social Insect: Effects of Heterozygosity on Immunocompetence in the Termite Zootermopsis Angusticollis Daniel V Proc. R. Soc. B (2006) 273, 2633–2640 doi:10.1098/rspb.2006.3622 Published online 18 July 2006 Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis Daniel V. Calleri II1,*, Ellen McGrail Reid1, Rebeca B. Rosengaus2, Edward L. Vargo3 and James F. A. Traniello1 1Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215-2406, USA 2Department of Biology, Northeastern University, 134 Mugar Life Science Building, 360 Huntington Avenue, Boston, MA 02115-5000, USA 3Department of Entomology, North Carolina State University, PO Box 7613, Raleigh, NC 27695-7613, USA Recent research has shown that low genetic variation in individuals can increase susceptibility to infection and group living may exacerbate pathogen transmission. In the eusocial diploid termites, cycles of outbreeding and inbreeding characterizing basal species can reduce genetic variation within nestmates during the life of a colony, but the relationship of genetic heterogeneity to disease resistance is poorly understood. Here we show that, one generation of inbreeding differentially affects the survivorship of isolated and grouped termites (Zootermopsis angusticollis) depending on the nature of immune challenge and treatment. Inbred and outbred isolated and grouped termites inoculated with a bacterial pathogen, exposed to a low dose of fungal pathogen or challenged with an implanted nylon monofilament had similar levels of immune defence. However, inbred grouped termites exposed to a relatively high concentration of fungal conidia had significantly greater mortality than outbred grouped termites. Inbred termites also had significantly higher cuticular microbial loads, presumably due to less effective grooming by nestmates. Genetic analyses showed that inbreeding significantly reduced heterozygosity and allelic diversity. Decreased heterozygosity thus appeared to increase disease susceptibility by affecting social behaviour or some other group-level process influencing infection control rather than affecting individual immune physiology. Keywords: isoptera; termite; life history; immunity; social behaviour 1. INTRODUCTION lower genetic variability at the individual level (Gerloff Decreased heterozygosity can arise from life-history traits et al. 2003; O’Donnell & Beshers 2004; Vainio et al. 2004; and impact disease resistance (Lively et al. 1990; Paterson Baer et al. 2005). Multiple mating can increase allelic et al. 1998; Lively et al. 2004; Pearman & Garner 2005). diversity and polyandry in bees and ants has been However, low heterozygosity does not compromise demonstrated to improve resistance to infection (Baer & parasite and pathogen resistance in a consistent manner Schmid-Hempel 1999; Baer & Schmid-Hempel 2001; across taxa (Hanley et al. 1995; Wiehn et al. 2002; Giese & Tarpy 2003; Denny et al. 2004; Hughes & Boomsma Hedrick 2003). In social insects, studies of the role of 2004). genetics in disease resistance must consider life-history Termites (order Isoptera), in contrast, are diploid and traits that increase the relatedness of colony members and typically monogamous and the life history of many basal decrease heterozygosity (Shykoff & Schmid-Hempel species is characterized by alternating generations of 1991). Enhanced disease exposure and transmission outbreeding and inbreeding that can alter heterozygosity rates thought to be associated with group living and high during a colony’s life cycle (Thorne 1997; Husseneder nestmate densities might further increase the risk of et al. 1999; Thorne et al. 1999; Vargo 2003; DeHeer & infection (Hamilton 1987; Rosengaus et al. 1998; Vargo 2004). Termite colonies generally are founded by Schmid-Hempel 1998). In monandrous ants, bees and dispersing winged primary reproductives followed by the wasps (order Hymenoptera), haplodiploid sex determina- development of secondary reproductives upon the death tion produces relatively high coefficients of relatedness of the primaries (Abe & Higashi 2001). Secondary that can increase the susceptibility of workers to infection reproductives may be full siblings that mate with each (Sherman et al.1988, 1998; Keller & Reeve 1994; other or a surviving parent (Thorne 1997), in either case Schmid-Hempel & Crozier 1999). Additionally, haploid contributing to colony growth through the production of males may be especially vulnerable to parasites due to their inbred offspring. Cycles of outbreeding by primary reproductives and inbreeding by secondary reproductives are considered to be significant in termite sociobiology * Author for correspondence ([email protected]). because of their consequences to nestmate relatedness Received 31 March 2006 2633 q 2006 The Royal Society Accepted 13 May 2006 2634 D. V. Calleri II and others Disease resistance in termites (Hamilton 1978; Thorne 1997; Roisin 1999). These (see §3a). Twenty-four colonies, each containing ca 200–500 cycles could involve disease-related costs of decreased individuals (nZ11 inbred colonies; nZ13 outbred colonies), heterozygosity associated with inbreeding (Thorne & provided termites for study. Inbred and outbred offspring Traniello 2003) and a pathogen-related increase in (pseudergates of instars IV–VII and nymphs) were hapha- mortality associated with outbreeding (Rosengaus & zardly removed from their nests and temporarily housed by Traniello 1993; Calleri et al. 2005). Because the immune colony in covered plastic boxes (15!10!6 cm) containing function of individuals and social interactions can both moist paper towel and nest wood. Individuals from all decrease the susceptibility of termite colonies to disease colonies were used in assays of immunocompetence within (Rosengaus et al. 1998, 1999a,b; Rosengaus & Traniello 5 days of removal from their parent colony. Fungal, bacterial 2001; Traniello et al. 2002), we examined immunocom- and nylon implant immune challenges for each colony petence in the broad sense of Owens & Wilson (1999) and occurred within this time period. measured a diverse array of individual- and group-level phenomena that could be involved in infection control. (b) Microsatellite variation, relatedness and genetic We experimentally evaluated whether heterozygosity in diversity individual pseudergates (‘false workers’) and nymphs of To estimate genetic variation and the degree of relatedness of the dampwood termite Zootermopsis angusticollis can inbred and outbred termites, individuals from each colony influence immune function and how it might affect disease (17.3G4.7, mean Gs.d., nZ24 colonies) were genotyped at resistance through its interaction with sociality. We five polymorphic microsatellite loci developed for Z. angusticollis assessed immunocompetence by recording the survivor- according to the methods described in Dronnet et al.(2005). ship of isolated and grouped termites challenged with Four loci consisted of dimers and one consisted of a tetramer. fungi, bacteria and a non-pathogenic immune inducer The microsatellites were amplified, run on a LiCor automated (a nylon implant). Additionally, we estimated cuticular sequencer and scored according to established methods (e.g., microbial loads of inbred and outbred offspring to index Vargo 2003). The number of alleles per locus ranged from three disease risk. We relate these measures of disease suscep- to six, with a mean (Gs.d.) of 4.2G1.3. The program FSTAT tibility to estimates of genetic variation in the inbred and v. 2.9.3.2 (Goudet 2001) was used to determine the average outbred offspring whose disease resistance we examined. number of alleles, observed heterozygosity and inbreeding Our results suggest that inbreeding may not impact coefficient (FIS) for each group. Standard errors for FIS were individual immunity, but may decrease the efficacy of estimated by jackknifing over loci. The coefficient of relatedness group-level processes of disease resistance. among siblings was estimated with the program RELATEDNESS v. 5.0.8 (Queller & Goodnight 1989), and standard errors were estimated by jackknifing over colonies. We used a one-tailed 2. MATERIAL AND METHODS t-test to determine if there were significant differences between (a) Colony establishment inbred and outbred colonies. Colonies of Z. angusticollis Hagen (nZ13, ca 200–1000 individuals/colony) were collected from sites separated by (c) Preparation of disease agents and experimental approximately 100 m in Palo Alto Foothill Park, Palo Alto, infections California. Log nests were transferred to plastic tubs (50! TheentomopathogenicfungusMetarhizium anisopliae 30!20 cm) lined with moist paper towels, regularly sprayed (original source: American Type Culture Collection, batch with water, and maintained in the laboratory at 25 8C. Alates 93-09, media 325, ATCC no. 90448) was used to (winged reproductives), which we used to establish inbred experimentally infect termites. This fungus naturally occurs and outbred colonies, emerged from most stock colonies with termites (Zoberi 1995) and has been cultured from within two months of collection. Z. angusticollis cadavers found in freshly collected field To create inbred and outbred colonies, we paired female colonies during a post-collection quarantine period (Calleri and male alates from the same stock colony (inbred, nZ22 et al. 2005, 2006). A detailed description of the preparation of pairs) or different stock colonies (outbred, nZ23 pairs). No Tween 80 conidia suspensions is given in Rosengaus et al. stock colony was used more than three times as a source
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