Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth

Tarpy, David R.

doi:10.1098/rspb.2002.2199

Cited by 309 publications

(261 citation statements)

References 52 publications

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“…Although the precise mechanisms may vary, this means there is now data supporting the genetic diversity/ disease resistance hypothesis in three species: Bombus terrestris (Shykoff and Schmid-Hempel 1991 ;Baer and SchmidHempel 1999, 2003, Apis mellifera Tarpy 2003), and Acromyrmex echinatior (this study). Any effect will depend upon the specific host-parasite interaction.…”

Section: Discussionmentioning

confidence: 94%

Genetic Diversity and Disease Resistance in Leaf-Cutting Ant Societies

Hughes

Boomsma

2004

Evol

112

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Abstract.•Multiple mating by females (polyandry) remains hard to explain because, while it has substantial costs, clear benefits have remained elusive. The problem is acute in the social insects because polyandry is probably particularly costly for females and most material benefits of the behavior are unlikely to apply. It has been suggested that a fitness benefit may arise from the more genetically diverse worker force that a polyandrous queen will produce. One leading hypothesis is that the increased genetic diversity of workers will improve a colony's resistance to disease. We investigated this hypothesis using a polyandrous leaf-cutting ant and a virulent fungal parasite as our model system. At high doses of the parasite most patrilines within colonies were similarly susceptible, but a few showed greater resistance. At a low dose of the parasite there was more variation between patrilines in their resistance to the parasite. Such genetic variation is a key prerequisite for polyandry to result in increased disease resistance of colonies. The relatedness of two hosts did not appear to affect the transmission of the parasite between them, but this was most likely because the parasite tested was a virulent generalist that is adapted to transmit between distantly related hosts. The resistance to the parasite was compared between small groups of ants of either high or low genetic diversity. No difference was found at high doses of the parasite, but a significant improvement in resistance in high genetic diversity groups was found at a low dose of the parasite. That there is genetic variation for disease resistance means that there is the potential for polyandry to produce more disease-resistant colonies. That this genetic variation can improve the resistance of groups even under the limited conditions tested suggests that polyandry may indeed produce colonies with improved resistance to disease.

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Section: Discussionmentioning

confidence: 94%

Genetic Diversity and Disease Resistance in Leaf-Cutting Ant Societies

Hughes

Boomsma

2004

Evol

112

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“…Given the well-established costs of immunity in insects and the consequent trade-offs between the immune response and other life history traits (Kraaijeveld and Godfray, 1997;Fellowes et al, 1998;Kraaijeveld et al, 2002;Rolff and SivaJothy, 2003;Schmid-Hempel, 2003;2005), genotypic differences in immunocompetence seem likely. Genetic variation for resistance has been found in several social insect species (Baer and Schmid-Hempel, 2003b;Palmer and Oldroyd, 2003;Tarpy, 2003;, although these results could relate to other defences as well as the immune system. Variation in the encapsulation response did not differ between males and females in either of the previous studies that compared the immunocompetence of social insect males and females (Gerloff et al, 2003;Vainio et al, 2004).…”

Section: Discussionmentioning

confidence: 96%

Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection

et al. 2005

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Summary. Parasites represent significant challenges to social insects. The high density, interaction rate and relatedness of individuals within colonies are all predicted to make social insect colonies particularly vulnerable to parasites. To cope with this pressure, social insects have evolved a number of defence mechanisms. These include the immune response, which, aside from in bumblebees, has been relatively little studied in social insects. Here we compare the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and examine the effect upon immunocompetence of prior exposure to a virulent parasite. Males have a far lower immune response than workers, suggesting either haploid susceptibility or reduced investment in immunity by the short-lived males. There was also significantly less variation in the immune response of males than of workers, which may be due to leaf-cutting ant workers being more variable in age or more genetically diverse within colonies. When exposed to the entomopathogenic fungus Metarhizium, workers expressed a substantially reduced immune response 96 h after infection, suggesting that the immune system was either depleted by having to respond to the Metarhizium infection or was depressed by the parasite. The results suggest that the immune response is a costly and limited process, but further experiments are needed to distinguish between the alternative explanations for the effects observed.

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“…First, the 'polyandry versus parasites' hypothesis states that increased genetic diversity within colonies enhances resistance to pathogens (Hamilton 1987;Sherman et al 1988;Keller & Reeve 1994). This has been shown in the ant A. echinatior and the honeybee Apis mellifera (Tarpy 2003;Tarpy & Seeley 2006). Also, in the bumblebee Bombus terrestris high-diversity colonies have fewer parasites and show greater reproductive success than do low-diversity colonies (Baer & Schmid-Hempel 1999.…”

Section: Discussionmentioning

confidence: 99%

Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor

et al. 2008

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Understanding the adaptive significance of multiple mating (polyandry) by females has long been a challenge in evolutionary biology. Several genetic and nongenetic benefits have been proposed to explain the evolution and maintenance of polyandry. In eusocial Hymenoptera, a prominent hypothesis is that increased genetic diversity within colonies results in more polymorphic workers and facilitates division of labour. We analysed the genetic basis of worker size (i.e. worker head width) and task preference in Cataglyphis cursor, an ant showing natural variations in queen-mating frequency. Our data show that increased genetic diversity within colonies does not result in more polymorphic workers. Moreover, worker head width is not different between patrilines within colonies. Consistent with these findings, worker size has a low heritable component. Moreover, task performance is not correlated with patriline. By contrast, it is significantly associated with worker size: the first foragers leaving the nest at sunrise are significantly larger than workers remaining in the nest. Overall, these results do not support the hypothesis that multiple mating is favoured because increased genetic diversity within colonies translates into more polymorphic workers and facilitates genetic polyethism. We discuss other hypotheses to account for the evolution of polyandry in C. cursor.

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Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth

Cited by 309 publications

References 52 publications

Genetic Diversity and Disease Resistance in Leaf-Cutting Ant Societies

Genetic Diversity and Disease Resistance in Leaf-Cutting Ant Societies

Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection

Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor

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