The role of male disease susceptibility in the evolution of haplodiploid insect societies

O’Donnell, Sean; Beshers, Samuel N.

doi:10.1098/rspb.2004.2685

Cited by 66 publications

(58 citation statements)

References 39 publications

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“…These results are interesting in light of recent studies of the effect of gender on immunocompetence that indicate that females in several taxa are more immunocompetent than males (reviewed by Roberts et al 2004). Gender-based differences in immunocompetence have been attributed to variation in male and female life-history traits and allelic variation in the Hymenoptera (Hamilton 1987;O'Donnell and Beshers 2004). Z. angusticollis and perhaps other termite species do not conform to these generalizations because males and females are diploid, have relatively long life expectancies (Schmid-Hempel 1998; Thorne et al 2002), cooperate in colony foundation, show parental care (Rosengaus and Traniello 1991;ShellmanReeve 1997), and participate in colony labor and defense.…”

Section: Discussionmentioning

confidence: 99%

Inducible immune proteins in the dampwood termite Zootermopsis angusticollis

Rosengaus

Cornelisse

Guschanski

et al. 2006

Naturwissenschaften

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Dampwood termites, Zootermopsis angusticollis (Isoptera: Termopsidae), mount an immune response to resist microbial infection. Here we report on results of a novel analysis that allowed us to electrophoretically assess changes in hemolymph proteins in the same individual before and after exposure to a pathogen. We demonstrate that contact with a sublethal concentration of the entomopathogenic fungus Metarhizium anisopliae (Deuteromycotina:Hypomycetes) induces the production of protective proteins in nymphs, pseudergates (false workers), and soldiers. Termites exposed to an immunizing dosage of fungal conidia consistently showed an enhancement of constitutive proteins (62-85 kDa) in the hemolymph as well as an induction of novel proteins (28-48 kDa) relative to preimmunization levels. No significant differences in protein banding patterns relative to baseline levels in control and naïve termites were observed. Incubating excised and eluted induced proteins produced by immunized pseudergates or immunized soldiers with conidia significantly reduced the germination of the fungus. The fungistatic effect of eluted proteins differed significantly among five colonies examined. Our results show that the upregulation of protective proteins in the hemolymph underscores the in vivo immune response we previously recorded in Z. angusticollis.

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Section: Discussionmentioning

confidence: 99%

Inducible immune proteins in the dampwood termite Zootermopsis angusticollis

Rosengaus

Cornelisse

Guschanski

et al. 2006

Naturwissenschaften

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“…Two different explanations have been put forward to explain compromised male immunity in hymenopteran social insects. The haplodiploid susceptibility hypothesis states that haploidy in social insect males reduces genetic variation in their immune system genes and consequently increases their disease susceptibility [24]. Alternatively, the trade-off hypothesis states that social insect males reallocate immunity-related investments to maximize fertility in order to satisfy the exceptionally high demands on sperm numbers and quality [25].…”

Section: Introductionmentioning

confidence: 99%

Seminal fluid of honeybees contains multiple mechanisms to combat infections of the sexually transmitted pathogen Nosema apis

Yan¹,

Grassl²,

Millar³

et al. 2016

Proc. R. Soc. B.

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The societies of ants, bees and wasps are genetically closed systems where queens only mate during a brief mating episode prior to their eusocial life and males therefore provide queens with a lifetime supply of high-quality sperm. These ejaculates also contain a number of defence proteins that have been detected in the seminal fluid but their function and efficiency have never been investigated in great detail. Here, we used the honeybee Apis mellifera and quantified whether seminal fluid is able to combat infections of the fungal pathogen Nosema apis, a widespread honeybee parasite that is also sexually transmitted. We provide the first empirical evidence that seminal fluid has a remarkable antimicrobial activity against N. apis spores and that antimicrobial seminal fluid components kill spores in multiple ways. The protein fraction of seminal fluid induces extracellular spore germination, which disrupts the life cycle of N. apis, whereas the non-protein fraction of seminal fluid induces a direct viability loss of intact spores. We conclude that males provide their ejaculates with efficient antimicrobial molecules that are able to kill N. apis spores and thereby reduce the risk of disease transmission during mating. Our findings could be of broader significance to master honeybee diseases in managed honeybee stock in the future.

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“…In monandrous ants, bees and wasps (order Hymenoptera), haplodiploid sex determination produces relatively high coefficients of relatedness that can increase the susceptibility of workers to infection (Sherman et al 1988(Sherman et al , 1998Keller & Reeve 1994;Schmid-Hempel & Crozier 1999). Additionally, haploid males may be especially vulnerable to parasites due to their lower genetic variability at the individual level (Gerloff et al 2003;O'Donnell & Beshers 2004;Vainio et al 2004;Baer et al 2005). Multiple mating can increase allelic diversity and polyandry in bees and ants has been demonstrated to improve resistance to infection (Baer & Schmid-Hempel 1999;Baer & Schmid-Hempel 2001;Tarpy 2003;Denny et al 2004;Hughes & Boomsma 2004).…”

Section: Introductionmentioning

confidence: 99%

Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis

et al. 2006

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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.

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The role of male disease susceptibility in the evolution of haplodiploid insect societies

Cited by 66 publications

References 39 publications

Inducible immune proteins in the dampwood termite Zootermopsis angusticollis

Inducible immune proteins in the dampwood termite Zootermopsis angusticollis

Seminal fluid of honeybees contains multiple mechanisms to combat infections of the sexually transmitted pathogen Nosema apis

Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis

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