Limits...
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

Sex ratio (proportion male) of populations of N. vitripennis in which superparasitism was permitted and host resources availability was high (top panel) or low (bottom panel).Black lines are individual replicate populations that were infected with A. nasoniae, grey lines are replicate control populations. A. nasoniae infection and spread caused significant deviation in sex ratio compared to uninfected controls (See Table 1). Furthermore, sex ratio varied considerable among infected populations in the same treatment group in many generations. Each treatment was run in two separate blocks of 3 replicates of both control and infected populations. Control populations were no longer maintained when all of their contemporary infected populations either lost the infection or went extinct.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4920596&req=5

ppat.1005629.g002: Sex ratio (proportion male) of populations of N. vitripennis in which superparasitism was permitted and host resources availability was high (top panel) or low (bottom panel).Black lines are individual replicate populations that were infected with A. nasoniae, grey lines are replicate control populations. A. nasoniae infection and spread caused significant deviation in sex ratio compared to uninfected controls (See Table 1). Furthermore, sex ratio varied considerable among infected populations in the same treatment group in many generations. Each treatment was run in two separate blocks of 3 replicates of both control and infected populations. Control populations were no longer maintained when all of their contemporary infected populations either lost the infection or went extinct.

Mentions: In treatments where superparasitism drove infection to high prevalence we also observed significant decreases in population sex ratio compared to uninfected controls (Fig 2 and Table 1). This effect varied in severity between generations and was asynchronous among replicate populations. Furthermore, five replicate populations in which infection increased and fly resources were low went extinct, most likely due to these sex ratio fluctuations. At generation eight, population extinction was significantly associated with the opportunity for wasps to superparasitise (Fisher’s exact test, P = 0.013), and low host resource (Fisher’s exact test P = 0.013)(Fig 3). Only a single uninfected control population under the same fly and parasitoid densities went extinct. This strongly indicates that symbiont induced sex-ratio bias is the major factor in eliciting host population crashes (control vs infected populations: Fisher’s exact test P = 0.015).


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)

Sex ratio (proportion male) of populations of N. vitripennis in which superparasitism was permitted and host resources availability was high (top panel) or low (bottom panel).Black lines are individual replicate populations that were infected with A. nasoniae, grey lines are replicate control populations. A. nasoniae infection and spread caused significant deviation in sex ratio compared to uninfected controls (See Table 1). Furthermore, sex ratio varied considerable among infected populations in the same treatment group in many generations. Each treatment was run in two separate blocks of 3 replicates of both control and infected populations. Control populations were no longer maintained when all of their contemporary infected populations either lost the infection or went extinct.
© Copyright Policy
Related In: Results  -  Collection

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

ppat.1005629.g002: Sex ratio (proportion male) of populations of N. vitripennis in which superparasitism was permitted and host resources availability was high (top panel) or low (bottom panel).Black lines are individual replicate populations that were infected with A. nasoniae, grey lines are replicate control populations. A. nasoniae infection and spread caused significant deviation in sex ratio compared to uninfected controls (See Table 1). Furthermore, sex ratio varied considerable among infected populations in the same treatment group in many generations. Each treatment was run in two separate blocks of 3 replicates of both control and infected populations. Control populations were no longer maintained when all of their contemporary infected populations either lost the infection or went extinct.
Mentions: In treatments where superparasitism drove infection to high prevalence we also observed significant decreases in population sex ratio compared to uninfected controls (Fig 2 and Table 1). This effect varied in severity between generations and was asynchronous among replicate populations. Furthermore, five replicate populations in which infection increased and fly resources were low went extinct, most likely due to these sex ratio fluctuations. At generation eight, population extinction was significantly associated with the opportunity for wasps to superparasitise (Fisher’s exact test, P = 0.013), and low host resource (Fisher’s exact test P = 0.013)(Fig 3). Only a single uninfected control population under the same fly and parasitoid densities went extinct. This strongly indicates that symbiont induced sex-ratio bias is the major factor in eliciting host population crashes (control vs infected populations: Fisher’s exact test P = 0.015).

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