Genetic diversity and genotypic differentiation between the sexes in swarm aggregations decrease inbreeding in the Formosan subterranean termite

The life of a colony of subterranean termites, such as Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), has natural inbreeding and outbreeding cycles. Reproductives of mature colonies can be replaced by their offspring, which increases the degree of inbreeding in each generation. High degrees of inbreeding may lead to inbreeding depression. In this study we focused on mechanisms for inbreeding avoidance during swarming that do not require kin recognition. We investigated genetic differentiation between swarm aggregations (isolation by distance), genetic diversity within swarm aggregations (multiple colony origin) and genetic differentiation between sexes. Alates were collected from five swarm aggregations in New Orleans, La. The genetic make-up of each swarm aggregation was then described by microsatellite genotyping. Alates from the different swarm aggregations were genetically differentiated; however, no isolation by distance up to at least 1000 m was detected. The dispersal distance of alates was sufficient to guarantee mixing of an average of 13 colonies within swarm aggregations. On average, eleven percent of all possible pairs of alates in each swarm aggregation were putative full siblings. Genotypic frequencies differed significantly between males and females. This could not be explained by sex-biased dispersal. We hypothesize sex-biased investment at the colony level to account for this difference. Genetic differentiation between the sexes and dispersal distances sufficient to promote high genetic diversity within swarm aggregations each facilitate inbreeding avoidance. These observations are consistent with the results of previous studies demonstrating that the majority of simple family colonies in Louisiana populations are headed by unrelated and outbred pairs of reproductives. Received 11 August 2005; revised 5 December 2005; accepted 20 December 2005.     

Seasonal patterns of population structure in a colonial marine invertebrate (Bugula stolonifera, Bryozoa)

For sessile invertebrates, the degree to which dispersal mechanisms transport individuals away from their natal grounds can have significant ecological implications. Even though the larvae of the marine bryozoan Bugula stolonifera have limited dispersal potential, high levels of genetic mixing have been found within their conspecific aggregations. In this study, we investigated whether this high mixing within aggregations of B. stolonifera also resulted in high mixing between aggregations. Adult colonies were collected from five sites within and one site outside of Eel Pond, Woods Hole, Massachusetts, in August 2009 and genotyped at 10 microsatellite loci. Significant genotypic differentiation was found between most sites, suggesting limited connectivity across sites, even those separated by only 100 m. This investigation was extended to determine if low levels of genetic mixing throughout the reproductive season could result in increased homogeneity between sites. Four of the five sites in Eel Pond were sampled early, mid-, and late in the reproductive season in 2010, and again in early 2011. Inter- and intra-annual genotypic differentiation was then assessed within and between sites. Results from these analyses document that low levels of mixing could result in increased homogeneity between some aggregations, but that barriers to genetic exchange prevented mixing between most sites. Further, results from inter-annual comparisons within sites suggest that any potential homogeneity achieved throughout the reproductive season will likely be lost by the beginning of the next reproductive season due to the annual cycle of colony die-back and regrowth experienced by B. stolonifera colonies in Eel Pond.     

Genetic structure of nest aggregations and drone congregations of the southeast Asian stingless bee Trigona collina

In stingless bees, sex is determined by a single complementary sex-determining locus. This method of sex determination imposes a severe cost of inbreeding because an egg fertilized by sperm carrying the same sex allele as the egg results in a sterile diploid male. To explore how reproductive strategies may be used to avoid inbreeding in stingless bees, we studied the genetic structure of a population of 27 colonies and three drone congregations of Trigona collina in Chanthaburi, Thailand. The colonies were distributed across six nest aggregations, each aggregation located in the base of a different fig tree. Genetic analysis at eight microsatellite loci showed that colonies within aggregations were not related. Samples taken from three drone congregations showed that the males were drawn from a large number of colonies (estimated to be 132 different colonies in our largest swarm). No drone had a genotype indicating that it could have originated from the colony that it was directly outside. Combined, these results suggest that movements of drones and possibly movements of reproductive swarms among colony aggregations provide two mechanisms of inbreeding avoidance.     

Contrasting genetic structuring between colonies of the World’s smallest penguin, <Emphasis Type="Italic">Eudyptula minor</Emphasis> (Aves: Spheniscidae)

The Little Penguin, Eudyptula minor, is a seabird that nests in colonies throughout New Zealand and southern Australia. Individuals from different colonies in southeast Australia differ significantly in morphology and ecology, suggesting that some genetic structuring may exist among colonies. In contrast, the marking of individuals with flipper bands has revealed some, albeit infrequent, movement between colonies. To determine the extent of genetic structuring, we tested the null hypothesis of substantial gene flow within southeast Australia by examining patterns of genetic variation across seven colonies separated by up to 1,500 km. Phylogeographic structuring was absent for mitochondrial control region sequences (2–3 individuals per colony). Microsatellite allele frequencies at five loci and mitochondrial haplotype frequencies (50 individuals per colony) were also homogenous among the majority of colonies sampled, although two colonies at the western periphery of the sampling range were distinct from those to the east. The genetic homogeneity among the majority of colonies can be explained by low but consistent contemporary gene flow among them, or a recent founder event in Bass Strait following the last marine transgression. The genetic break towards the western end of the sampling distribution appears best explained by differences in sea surface temperature and, consequentially breeding phenology, the latter hindering genetically effective migration.     

Natural variation in colony inbreeding does not influence susceptibility to a fungal pathogen in a termite

Reduced genetic diversity through inbreeding can negatively affect pathogen resistance. This relationship becomes more complicated in social species, such as social insects, since the chance of disease transmission increases with the frequency of interactions among individuals. However, social insects may benefit from social immunity, whereby individual physiological defenses may be bolstered by collective‐level immune responses, such as grooming or sharing of antimicrobial substance through trophallaxis. We set out to determine whether differences in genetic diversity between colonies of the subterranean termite, Reticulitermes flavipes, accounts for colony survival against pathogens. We sampled colonies throughout the United States (Texas, North Carolina, Maryland, and Massachusetts) and determined the level of inbreeding of each colony. To assess whether genetically diverse colonies were better able to survive exposure to diverse pathogens, we challenged groups of termite workers with two strains of a pathogenic fungus, one local strain present in the soil surrounding sampled colonies and another naïve strain, collected outside the range of this species. We found natural variation in the level of inbreeding between colonies, but this variation did not explain differences in susceptibility to either pathogen. Although the naïve strain was found to be more hazardous than the local strain, colony resistance was correlated between two strains, meaning that colonies had either relatively high or low susceptibility to both strains regardless of their inbreeding coefficient. Overall, our findings may reflect differential virulence between the strains, immune priming of the colonies via prior exposure to the local strain, or a coevolved resistance toward this strain. They also suggest that colony survival may rely more upon additional factors, such as different behavioral response thresholds or the influence of a specific genetic background, rather than the overall genetic diversity of the colony.     

Sylvatic plague reduces genetic variability in black-tailed prairie dogs

Small, isolated populations are vulnerable to loss of genetic diversity through in-breeding and genetic drift. Sylvatic plague due to infection by the bacterium Yersinia pestis caused an epizootic in the early 1990s resullting in declines and extirpations of many black-tailed prairie dog (Cynomys ludovicianus) colonies in north-central Montana, USA. Plague-induced population bottlenecks may contribute to significant reductions in genetic variability. In contrast, gene flow maintains genetic variability within colonies. We investigated the impacts of the plague epizootic and distance to nearest colony on levels of genetic variability in six prairie dog colonies sampled between June 1999 and July 2001 using 24 variable randomly amplified polymorphic DNA (RAPD) markers. Number of effective alleles per locus (n(e)) and gene diversity (h) were significantly decreased in the three colonies affected by plague that were recovering from the resulting bottlenecks compared with the three colonies that did not experience plague. Genetic variability was not significantly affected by geographic distance between colonies. The majority of variance in gene fieqnencies was found within prairie clog colonies. Conservation of genetic variability in black-tailed prairie dogs will require the preservation of both large and small colony complexes and the gene flow amonog them.     

Colony interactions in <Emphasis Type="Italic">Reticulitermes grassei</Emphasis> population assessed by molecular genetic methods

The cryptic habits of subterranean termites impair studies of colony delimitation and the organization of foraging. Whereas feeding sites can be identified and the movements of foragers between them can be assessed using traditional mark-release techniques, the assignment of the termites found at feeding sites to their parent colonies remains problematical. Thus the extent and overlap of individual colony foraging territories are unknown. We used microsatellite markers to delineate colonies of R. grassei and compared the results with data from a mark-release-recapture study (Nobre et al., 2007) carried out in the same population and over the same period of time. The majority of colonies exhibited only a single-feeding site, but presented, even at a local scale, a high degree of variability in colony structure and no evidence of inbreeding. F-statistics for some colonies were consistent with pleometrosis. The population as a whole contained individual colonies that were separately identified as Mendelian, mixed family or pleometrotic families. Furthermore, microsatellite data suggest that what was represented by the MRR technique as a single foraging group could be drawn from more than one colony. Colony delineation is discussed as a tool for understanding overall population structure and termite feeding strategies. Received 5 July; revised 3 October 2007; accepted 19 October 2007.     

Spatial structuring of the population genetics of a European subterranean termite species

In population genetics studies, detecting and quantifying the distribution of genetic variation can help elucidate ecological and evolutionary processes. In social insects, the distribution of population‐level genetic variability is generally linked to colony‐level genetic structure. It is thus especially crucial to conduct complementary analyses on such organisms to examine how spatial and social constraints interact to shape patterns of intraspecific diversity. In this study, we sequenced the mitochondrial COII gene for 52 colonies of the subterranean termite Reticulitermes grassei (Isoptera: Rhinotermitidae), sampled from a population in southwestern France. Three haplotypes were detected, one of which was found exclusively in the southern part of the study area (near the Pyrenees). After genotyping 6 microsatellite loci for 512 individual termites, we detected a significant degree of isolation by distance among individuals over the entire range; however, the cline of genetic differentiation was not continuous, suggesting the existence of differentiated populations. A spatial principal component analysis based on allele frequency data revealed significant spatial autocorrelation among genotypes: the northern and southern groups were strongly differentiated. This finding was corroborated by clustering analyses; depending on the randomized data set, two or three clusters, exhibiting significant degrees of differentiation, were identified. An examination of colony breeding systems showed that colonies containing related neotenic reproductives were prevalent, suggesting that inbreeding may contribute to the high level of homozygosity observed and thus enhance genetic contrasts among colonies. We discuss the effect of evolutionary and environmental factors as well as reproductive and dispersal modes on population genetic structure.     

Variation in reproductive characteristics of colonies of the freshwater bryozoan Cristatella mucedo

1. We studied relationships between different forms of reproduction and local variation in the reproductive state of colonies of a common freshwater bryozoan Cristatella mucedo Cuvier (Bryozoa: Phylactolaemata). Four sampling locations in central Finland, including both lotic and lentic habitats, were sampled by scuba diving. The traits studied were occurrence of sexual larvae, colony size, number of resting stages (statoblasts) and number of zooids. 2. While 76.9% of the sampled colonies carried statoblasts at the time of sampling, only 4.5% of the colonies were brooding sexual larvae. Most of the colonies were relatively small with a mean colony size of 16.6 mm. 3. In colonies brooding larvae, the number of statoblasts was positively correlated with the number of larvae. We did not detect a colony size threshold for sexual reproduction or formation of statoblasts. Colonies carrying statoblasts had a lower number of zooids per unit dry weight. 4. We found significant variation in reproductive traits of colonies among the sampling locations, and among lotic and lentic habitats. The observed phenotypic differences may reflect broadly distributed, phenotypically plastic clones. Differences in clonal composition of local populations cannot, however, be ruled out and factors that may provide clonal diversity are discussed.     

Genetic structure of an Apis dorsata population: the significance of migration and colony aggregation

Eight microsatellite loci were used to investigate the genetic structure of the giant honeybee (Apis dorsata) population in northeast India. This species migrates seasonally between summer and winter nesting sites, and queens appear to return to their previously occupied site. Furthermore, there is a strong tendency for colonies of this species to aggregate at perennially utilized nesting sites that may be shared by more than 150 colonies. These behavioral features suggest that colonies within aggregations should be more related than random colonies, but that the long-distance migration could act to minimize genetic differentiation both between geographical areas and within aggregations. Our genetic study supports these conjectures arising from natural history. A. dorsata aggregations are comprised of colonies that share more alleles than expected by chance. Although queens heading neighboring colonies are not close relatives, fixation indices show significant genetic differentiation among aggregation sites. However, there appears to be sufficient gene flow among aggregations to prevent high degrees of relatedness developing between colonies within aggregations. The results also suggest that there is significant population structuring between geographical regions, although the level of structuring caused by aggregation exceeds the differentiation attributable to geographic region.     

Inbreeding depression in ring-tailed lemurs (<Emphasis Type="Italic">Lemur catta</Emphasis>): genetic diversity predicts parasitism,immunocompetence, and survivorship

The consequences of inbreeding have been well studied in a variety of taxa, revealing that inbreeding has major negative impacts in numerous species, both in captivity and in the wild; however, as trans-generational health data are difficult to obtain for long-lived, free-ranging species, similar analyses are generally lacking for nonhuman primates. Here, we examined the long-term effects of inbreeding on numerous health estimates in a captive colony of ring-tailed lemurs (Lemur catta), housed under semi-natural conditions. This vulnerable strepsirrhine primate is endemic to Madagascar, a threatened hotspot of biodiversity; consequently, this captive population represents an important surrogate. Despite significant attention to maintaining the genetic diversity of captive animals, breeding colonies invariably suffer from various degrees of inbreeding. We used neutral heterozygosity as an estimate of inbreeding and showed that our results reflect genome-wide inbreeding, rather than local genetic effects. In particular, we found that genetic diversity affects several fitness correlates, including the prevalence and burden of Cuterebra parasites and a third (N = 6) of the blood parameters analyzed, some of which reflect immunocompetence. As a final validation of inbreeding depression in this captive colony, we showed that, compared to outbred individuals, inbred lemurs were more likely to die earlier from diseases. Through these analyses, we highlight the importance of monitoring genetic variation in captive animals—a key objective for conservation geneticists—and provide insight into the potential negative consequences faced by small or isolated populations in the wild. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Effects of honey bees on colonies of Exoneura asimillima,an Australian native bee

Honey bee hives were placed, during two consecutive summers, in an experimental site which contained natural and artificially placed colonies of Exoneura asimillima, a semi-social, native bee. Two classes of colonies were studied: founders, and established colonies. Nests and contents were collected from an experimental site and three control sites following several months of exposure at the experimental site to the apiary honey bee population. Nest contents were analysed for differences among sites in colony population parameters which could have been caused by resource competition with introduced honey bees. Colony founding and overall colony survival were also considered. During the first season, the average number of large larvae plus prepupae per colony was significantly higher in the experimental site than in the control site. This difference could, however, have been the result of a two-week gap in sampling all the sites. All nest parameters showed high variability and there were no other significant differences between the two kinds of site. In the experimental site during the second season there were, relative to the control sites, significantly fewer total numbers of adult males and females in established nests and in all nests combined, significantly more immatures of all stages in founder nests and significantly lower adult male:female ratio. Although preliminary in nature, the data suggest that, in the experimental plots, E. asimillima showed: (i) increased adult emigration, (ii) increased brood rearing success, and/or (iii) relatively later colony founding, compared to the three controls. The possibility of resource competiton with honey bees causing the observed changes is discussed, along with alternative explanations.     

Restricted mating dispersal and strong breeding group structure in a mid-sized marsupial mammal (Petrogale penicillata)

Ecological genetic studies have demonstrated that spatial patterns of mating dispersal, the dispersal of gametes through mating behaviour, can facilitate inbreeding avoidance and strongly influence the structure of populations, particularly in highly philopatric species. Elements of breeding group dynamics, such as strong structuring and sex-biased dispersal among groups, can also minimize inbreeding and positively influence levels of genetic diversity within populations. Rock-wallabies are highly philopatric mid-sized mammals whose strong dependence on rocky terrain has resulted in series of discreet, small colonies in the landscape. Populations show no signs of inbreeding and maintain high levels of genetic diversity despite strong patterns of limited gene flow within and among colonies. We used this species to investigate the importance of mating dispersal and breeding group structure to inbreeding avoidance within a 'small' population. We examined the spatial patterns of mating dispersal, the extent of kinship within breeding groups, and the degree of relatedness among brush-tailed rock-wallaby breeding pairs within a colony in southeast Queensland. Parentage data revealed remarkably restricted mating dispersal and strong breeding group structuring for a mid-sized mammal. Breeding groups showed significant levels of female kinship with evidence of male dispersal among groups. We found no evidence for inbreeding avoidance through mate choice; however, anecdotal data suggest the importance of life history traits to inbreeding avoidance between first-degree relatives. We suggest that the restricted pattern of mating dispersal and strong breeding group structuring facilitates inbreeding avoidance within colonies. These results provide insight into the population structure and maintenance of genetic diversity within colonies of the threatened brush-tailed rock-wallaby.     

Colony social organization and population genetic structure of an introduced population of formosan subterranean termite from New Orleans, Louisiana

The Formosan subterranean termite, Coptotermes formosanus Shiraki, is an invasive species in many parts of the world, including the U.S. mainland. The reasons for its invasive success may have to do with the flexible social and spatial organization of colonies. We investigated the population and breeding structure of 14 C. formosanus colonies in Louis Armstrong Park, New Orleans, LA. This population has been the focus of extensive study for many years, providing the opportunity to relate aspects of colony breeding structure to previous findings on colony characteristics such as body weight and number of workers, wood consumption, and intercolony aggression. Eight colonies were headed by a single pair of outbred reproductives (simple families), whereas six colonies were headed by low numbers of multiple kings and/or queens that were likely the neotenic descendants of the original colony (extended families). Within the foraging area of one large extended family colony, we found genetic differentiation among different collection sites, suggesting the presence of separate reproductive centers. No significant difference between simple family colonies and extended family colonies was found in worker body weight, soldier body weight, foraging area, population size, or wood consumption. However, level of inbreeding within colonies was negatively correlated with worker body weight and positively correlated with wood consumption. Also, genetic distance between colonies was positively correlated with aggression levels, suggesting a genetic basis to nestmate discrimination cues in this termite population. No obvious trait associated with colony reproductive structure was found that could account for the invasion success of this species.     

Clonal diversity impacts coral cover in Acropora cervicornis thickets: Potential relationships between density,growth, and polymorphisms

As coral reefs decline, cryptic sources of resistance and resilience to stress may be increasingly important for the persistence of these communities. Among these sources, inter‐ and intraspecific diversity remain understudied on coral reefs but extensively impact a variety of traits in other ecosystems. We use a combination of field and sequencing data at two sites in Florida and two in the Dominican Republic to examine clonal diversity and genetic differentiation of high‐ and low‐density aggregations of the threatened coral Acropora cervicornis in the Caribbean. We find that high‐density aggregations called thickets are composed of up to 30 genotypes at a single site, but 47% of genotypes are also found as isolated, discrete colonies outside these aggregations. Genet–ramet ratios are comparable for thickets (0.636) and isolated colonies after rarefaction (0.569), suggesting the composition of each aggregation is not substantially different and highlighting interactions between colonies as a potential influence on structure. There are no differences in growth rate, but a significant positive correlation between genotypic diversity and coral cover, which may be due to the influence of interactions between colonies on survivorship or fragment retention during asexual reproduction. Many polymorphisms distinguish isolated colonies from thickets despite the shared genotypes found here, including putative nonsynonymous mutations that change amino acid sequence in 25 loci. These results highlight intraspecific diversity as a density‐dependent factor that may impact traits important for the structure and function of coral reefs.     

Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching

Understanding the pattern of connectivity among populations is crucial for the development of realistic and spatially explicit population models in marine systems. Here we analysed variation at eight microsatellite loci to assess the genetic structure and to infer patterns of larval dispersal for a brooding coral, Seriatopora hystrix, at an isolated system of reefs in northern Western Australia. Spatial autocorrelation analyses show that populations are locally subdivided, and that the majority of larvae recruit to within 100 m of their natal colony. Further, a combination of F- and R- statistics showed significant differentiation at larger spatial scales (2-60 km) between sites, and this pattern was clearly not associated with distance. However, Bayesian analysis demonstrated that recruitment has been supplemented by less frequent but recent input of larvae from outside the local area; 2-6% of colonies were excluded from the site at which they were sampled. Individual assignments of these migrants to the most likely populations suggest that the majority of migrants were produced at the only site that was not decimated by a recent and catastrophic coral bleaching event. Furthermore, the only site that recovered to prebleaching levels received most of these immigrants. We conclude that the genetic structure of this brooding coral reflects its highly opportunistic life history, in which prolific, philopatric recruitment is occasionally supplemented by exogenously produced larvae.     

Nest Suitability,Fine-Scale Population Structure and Male-Mediated Dispersal of a Solitary Ground Nesting Bee in an Urban Landscape

Bees are the primary pollinators of flowering plants in almost all ecosystems. Worldwide declines in bee populations have raised awareness about the importance of their ecological role in maintaining ecosystem functioning. The naturally strong philopatric behavior that some bee species show can be detrimental to population viability through increased probability of inbreeding. Furthermore, bee populations found in human-altered landscapes, such as urban areas, can experience lower levels of gene flow and effective population sizes, increasing potential for inbreeding depression in wild bee populations. In this study, we investigated the fine-scale population structure of the solitary bee Colletes inaequalis in an urbanized landscape. First, we developed a predictive spatial model to detect suitable nesting habitat for this ground nesting bee and to inform our field search for nests. We genotyped 18 microsatellites in 548 female individuals collected from nest aggregations throughout the study area. Genetic relatedness estimates revealed that genetic similarity among individuals was slightly greater within nest aggregations than among randomly chosen individuals. However, genetic structure among nest aggregations was low (Nei’s G_ST = 0.011). Reconstruction of parental genotypes revealed greater genetic relatedness among females than among males within nest aggregations, suggesting male-mediated dispersal as a potentially important mechanism of population connectivity and inbreeding avoidance. Size of nesting patch was positively correlated with effective population size, but not with other estimators of genetic diversity. We detected a positive trend between geographic distance and genetic differentiation between nest aggregations. Our landscape genetic models suggest that increased urbanization is likely associated with higher levels of inbreeding. Overall, these findings emphasize the importance of density and distribution of suitable nesting patches for enhancing bee population abundance and connectivity in human dominated habitats and highlights the critical contribution of landscape genetic studies for enhanced conservation and management of native pollinators.     

Inbreeding and reproductive investment in the ant Formica exsecta

In social animals, inbreeding depression may manifest by compromising care or resources individuals receive from inbred group members. We studied the effects of worker inbreeding on colony productivity and investment in the ant Formica exsecta. The production of biomass decreased with increasing inbreeding, as did biomass produced per worker. Inbred colonies produced fewer gynes (unmated reproductive females), whereas the numbers of males remained unchanged. As a result, sex ratios showed increased male bias, and the fraction of workers increased among the diploid brood. Males raised in inbred colonies were smaller, whereas the weight of gynes remained unchanged. The results probably reflect a trade-off between number and quality of offspring, which is expected if the reproductive success of gynes is more dependent on their weight or condition than it is for males. As males are haploid (with the exception of abnormal diploid males produced in very low frequencies in this population), and therefore cannot be inbred themselves, the effect on their size must be mediated through the workers of the colony. We suggest the effects are caused by the inbred workers being less proficient in feeding the growing larvae. This represents a new kind of social inbreeding depression that may affect sex ratios as well as caste fate in social insects.     

Evaluation of DNA Fingerprinting, Aggression Tests, and Morphometry as Tools for Colony Delineation of the Formosan Subterranean Termite

Multilocus DNA fingerprinting, aggression tests, and morphometry were compared to evaluate their potential for the delineation of colonies of Coptotermes formosanus Shiraki (Isoptera; Rhinotermitidae) in Hawaii. DNA fingerprinting segregates the termites from all collection sites and allows the assignment of all individuals to their original collection site. The genetic similarity of termites from different collection sites approaches the population's genetic background similarity, consequently collection sites represent independent colonies. Aggression between colonies is comparatively low and does not provide reliable colony delineation. Morphometry allows a 79% classification rate of termites to their colony of origin. No correlation among genetic similarities, aggression levels, and morphometric distances is found. Of the three investigated methods, we conclude that the genetic approach is the most useful tool for colony delineation in C. formosanus.     

Intracolonial genetic variability in honeybee larval resistance to the chalkbrood and American foulbrood parasites

The origin of multiple mating of queens in social Hymenoptera is a widely debated topic in evolutionary biology. One of the hypotheses is that genetic variability would benefit the colony by increasing its resistance to parasites through various mechanisms. One among the predictions of this hypothesis is that the resistance of different patrilines within a colony to parasites of different species should be independent, as a result of independent gene-for-gene interactions with each parasite. To test this aspect of the hypothesis, two honeybee colonies (Apis mellifera) were infected with the fungus Ascosphaera apis and two colonies with both A. apis and the American foulbrood bacterium Paenibacillus larvae. Patrilines were found to vary in resistance of larvae to A. apis in all four colonies, but similar variation in resistance was not found to P. larvae. Common resistance to both pathogens was not detected. This study supports the hypothesis that polyandry in social insects could have originated as an adaptation to decrease the impact of diseases.