GENETIC DIVERSITY AND DISEASE RESISTANCE IN LEAF-CUTTING ANT SOCIETIES (original) (raw)
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Experimentally increased group diversity improves disease resistance in an ant species
Ecology Letters, 2008
A leading hypothesis linking parasites to social evolution is that more genetically diverse social groups better resist parasites. Moreover, group diversity can encompass factors other than genetic variation that may also influence disease resistance. Here, we tested whether group diversity improved disease resistance in an ant species with natural variation in colony queen number. We formed experimental groups of workers and challenged them with the fungal parasite Metarhizium anisopliae. Workers originating from monogynous colonies (headed by a single queen and with low genetic diversity) had higher survival than workers originating from polygynous ones, both in uninfected groups and in groups challenged with M. anisopliae. However, an experimental increase of group diversity by mixing workers originating from monogynous colonies strongly increased the survival of workers challenged with M. anisopliae, whereas it tended to decrease their survival in absence of infection. This experiment suggests that group diversity, be it genetic or environmental, improves the mean resistance of group members to the fungal infection, probably through the sharing of physiological or behavioural defences.
Proceedings of the Royal Society B: Biological Sciences
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.
Does genetic diversity hinder parasite evolution in social insect colonies?
Journal of Evolutionary Biology, 2006
Polyandry is often difficult to explain because benefits of the behaviour have proved elusive. In social insects, polyandry increases the genetic diversity of workers within a colony and this has been suggested to improve the resistance of the colony to disease. Here we examine the possible impact of host genetic diversity on parasite evolution by carrying out serial passages of a virulent fungal pathogen through leaf-cutting ant workers of known genotypes. Parasite virulence increased over the nine-generation span of the experiment while spore production decreased. The effect of host relatedness upon virulence appeared limited. However, parasites cycled through more genetically diverse hosts were more likely to go extinct during the experiment and parasites cycled through more genetically similar hosts had greater spore production. These results indicate that host genetic diversity may indeed hinder the ability of parasites to adapt while cycling within social insect colonies. Genetic diversity vs. parasite evolution 143 J . E V O L . B I O L . 1 9 ( 2 0 0 6 ) 1 3 2 -1 4 3 ª 2 0 0 5 E U R O P E
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. K E Y W O R D S Blattodea, diversity, Metarhizium, Reticulitermes flavipes, Rhinotermitidae, social immunity
Genetic diversity, paternal origin and pathogen resistance in Cataglyphis desert ants
Group diversity is usually associated with a reduced risk of disease outbreak and a slower rate of pathogen transmission. In social insects, multiple mating by queens (polyandry) evolved several times although reducing worker’s inclusive fitness. One major hypothesis suggests that polyandry has been selected for to mitigate the risk of outbreak thanks to increased genetic diversity within colonies. We investigated this hypothesis in the ant Cataglyphis mauritanica, in which nestmate workers are produced by several clonal, single-mated queens. Using natural colonies, we correlated genetic diversity with worker survival to a fungal entomopathogen. We further tested whether workers from different paternal lineages (but a common maternal genome) show differential resistance in experimentally singleor multiple-patriline groups, and whether an increased number of patrilines in a group improved disease incidence.We show that workers from distinct patrilines vary in their resistance to path...
2019
Polyandry (multiple mating by females) is a central challenge for understanding the evolution of eusociality. Several hypotheses have been proposed to explain its observed benefits in eusocial Hymenoptera, and one, the parasite–pathogen hypothesis, proposes that high genotypic variance among workers for disease resistance prevents catastrophic colony collapse. We tested the parasite–pathogen hypothesis in the polyandrous wasp Vespula shidai. We infected isolated workers with the entomopathogenic fungus Beauveria bassiana and quantified their survival in the laboratory. Additionally, we conducted paternity analysis of the workers using nine microsatellite loci to investigate the relationship between survival and matriline/patriline of the workers. As predicted by the parasite–pathogen hypothesis, nestmate workers of different patrilines showed differential resistance to B. bassiana. We also demonstrated variations in virulence among strains of B. bassiana. Our results are the first t...
Proceedings of the Royal Society of London B, 2006
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.
Genetic, Individual, and Group Facilitation of Disease Resistance in Insect Societies
Annual Review of Entomology, 2009
In this review, we provide a current reference on disease resistance in insect societies. We start with the genetics of immunity in the context of behavioral and physiological processes and scale up levels of biological organization until we reach populations. A significant component of this review focuses on Apis mellifera and its role as a model system for studies on social immunity. We additionally review the models that have been applied to disease transmission in social insects and elucidate areas for future study in the field of social immunity. 405 Annu. Rev. Entomol. 2009.54:405-423. Downloaded from arjournals.annualreviews.org by 76.17.242.162 on 12/24/08. For personal use only. Click here for quick links to Annual Reviews content online, including: • Other articles in this volume • Top cited articles • Top downloaded articles • Our comprehensive search Further ANNUAL REVIEWS Social immunity: collective defenses against parasites and pathogens IC: immunocompetence Immunity: traits that decrease susceptibility to parasites and pathogens Antiseptic behavior: behavioral traits that decrease disease transmission and susceptibility 406 Wilson-Rich et al. Annu. Rev. Entomol. 2009.54:405-423. Downloaded from arjournals.annualreviews.org by 76.17.242.162 on 12/24/08. For personal use only. www.annualreviews.org • Disease Resistance in Insect Societies 407 Annu. Rev. Entomol. 2009.54:405-423. Downloaded from arjournals.annualreviews.org by 76.17.242.162 on 12/24/08. For personal use only. www.annualreviews.org • Disease Resistance in Insect Societies 409 Annu. Rev. Entomol. 2009.54:405-423. Downloaded from arjournals.annualreviews.org by 76.17.242.162 on 12/24/08. For personal use only. Annu. Rev. Entomol. 2009.54:405-423. Downloaded from arjournals.annualreviews.org by 76.17.242.162 on 12/24/08. For personal use only.
BMC Ecology and Evolution, 2021
Background The ‘genetic diversity’ hypothesis posits that polyandry evolved as a mechanism to increase genetic diversity within broods. One extension of this hypothesis is the ‘genetic diversity for disease resistance’ hypothesis (GDDRH). Originally designed for eusocial Hymenoptera, GDDRH states that polyandry will evolve as an effect of lower parasite prevalence in genetically variable broods. However, this hypothesis has been broadly applied to several other taxa. It is unclear how much empirical evidence supports GDDRH specifically, especially outside eusocial Hymenoptera. Results This question was addressed by conducting a literature review and posteriorly conducting meta-analyses on the data available using Hedges’s g . The literature review found 10 direct and 32 indirect studies with both having a strong publication bias towards Hymenoptera. Two meta-analyses were conducted and both found increased polyandry (direct tests; n = 8, g = 0.2283, p = < 0.0001) and genetic ...