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Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp.

Parratt SR, Frost CL, Schenkel MA, Rice A, Hurst GD, King KC - PLoS Pathog. (2016)

Bottom Line: Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts.We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts.The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence.

View Article: PubMed Central - PubMed

Affiliation: Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

ABSTRACT
Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont's spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that 'reproductive parasite' phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections.

No MeSH data available.


Related in: MedlinePlus

Prevalence of A. nasoniae in populations of N. vitripennis kept under varying opportunities to superparasitise for four generations.All populations were started with 50% prevalence of A. nasoniae (dotted lines). The trend line is fitted from predictions of a binomially distributed GLM.
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ppat.1005629.g004: Prevalence of A. nasoniae in populations of N. vitripennis kept under varying opportunities to superparasitise for four generations.All populations were started with 50% prevalence of A. nasoniae (dotted lines). The trend line is fitted from predictions of a binomially distributed GLM.

Mentions: Infection prevalence after four generations was observed to be significantly, positively associated with superparasitism opportunity (comparison of binomial GLMMs, χ2 = 30.154, df = 1, P<0.001, Fig 4). In all cases the final infection prevalence significantly deviated from the starting prevalence of 50%. Prevalence increased where 50% or more wasps had the opportunity to superparasitise, and reduced where superparasitism was possible for 30% or fewer wasps (exact binomial test, P <0.001 in all cases, Fig 4).


Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp.

Parratt SR, Frost CL, Schenkel MA, Rice A, Hurst GD, King KC - PLoS Pathog. (2016)

Prevalence of A. nasoniae in populations of N. vitripennis kept under varying opportunities to superparasitise for four generations.All populations were started with 50% prevalence of A. nasoniae (dotted lines). The trend line is fitted from predictions of a binomially distributed GLM.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4920596&req=5

ppat.1005629.g004: Prevalence of A. nasoniae in populations of N. vitripennis kept under varying opportunities to superparasitise for four generations.All populations were started with 50% prevalence of A. nasoniae (dotted lines). The trend line is fitted from predictions of a binomially distributed GLM.
Mentions: Infection prevalence after four generations was observed to be significantly, positively associated with superparasitism opportunity (comparison of binomial GLMMs, χ2 = 30.154, df = 1, P<0.001, Fig 4). In all cases the final infection prevalence significantly deviated from the starting prevalence of 50%. Prevalence increased where 50% or more wasps had the opportunity to superparasitise, and reduced where superparasitism was possible for 30% or fewer wasps (exact binomial test, P <0.001 in all cases, Fig 4).

Bottom Line: Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts.We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts.The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence.

View Article: PubMed Central - PubMed

Affiliation: Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

ABSTRACT
Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont's spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that 'reproductive parasite' phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections.

No MeSH data available.


Related in: MedlinePlus