Manipulation of Arthropod Sex Determination by Endosymbionts: Diversity and Molecular Mechanisms

Ma, Wen‐Juan; Vavre, Fabrice; Beukeboom, Leo W.

doi:10.1159/000357024

Cited by 51 publications

(59 citation statements)

References 127 publications

(169 reference statements)

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“…Heritable bacterial endosymbionts are widespread in arthropods. They utilize diverse strategies to spread within host populations, such as provision of essential nutrients (Gündüz & Douglas, ; Hosokawa, Koga, Kikuchi, Meng, & Fukatsu, ), defense against parasites (Hedges, Brownlie, O'Neill, & Johnson, ; Vorburger, Gehrer, & Rodriguez, ), and reproductive manipulation (Ma, Vavre, & Beukeboom, ).…”

Section: Introductionmentioning

confidence: 99%

Symbiont‐conferred reproduction and fitness benefits can favour their host occurrence

Zhang

Yang

Zhu

et al. 2018

Ecology and Evolution

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Double infections of Wolbachia and Spiroplasma are frequent in natural populations of Tetranychus truncatus, a polyphagous mite species that has been a dominant species in China since 2009. However, little is known about the causes and ecological importance of such coexistences. In this study, we established T. truncatus strains with different infection types and then inferred the impact of the two endosymbionts on host reproduction and fitness. Double infection induced cytoplasmic incompatibility, which was demonstrated by reduction in egg hatchability of incompatible crosses. However, doubly infected females produced more eggs relative to other strains. Wolbachia and Spiroplasma did not affect host survival, whereas doubly infected females and males developed faster than other strains. Such reproduction and fitness benefits provided by double infections may be associated with the lower densities of each symbiont, and the quantitative results also confirmed competition between Wolbachia and Spiroplasma in doubly infected females. These symbiont‐conferred beneficial effects maintain stable prevalence of the symbionts and also help drive T. truncatus outbreaks in combination with other environmental factors.

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Section: Introductionmentioning

confidence: 99%

Symbiont‐conferred reproduction and fitness benefits can favour their host occurrence

Zhang

Yang

Zhu

et al. 2018

Ecology and Evolution

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“…An exception to this constraint applies to those species in which asexuality is induced by infection with bacterial endosymbionts, such as A. japonica (Kremer et al , 2009; Reumer et al , 2012). Endosymbiont-induced asexuality is mainly found among wasps and among other groups in which sexual species are characterized by haplodiploid sex determination (Werren, 1997; Werren et al , 2008; Mateo Leach et al , 2009; Giorgini et al , 2010; Kageyama et al , 2012; Ma et al , 2014), although it has also been suggested to occur in species with other sex determination systems (for example, Pike and Kingcombe, 2009). Under haplodiploidy, females develop from fertilized, diploid eggs, whereas males develop from unfertilized, haploid eggs (Whiting, 1933).…”

Section: Introductionmentioning

confidence: 99%

Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality

Pannebakker

Beukeboom

et al. 2014

Heredity

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Trait decay may occur when selective pressures shift, owing to changes in environment or life style, rendering formerly adaptive traits non-functional or even maladaptive. It remains largely unknown if such decay would stem from multiple mutations with small effects or rather involve few loci with major phenotypic effects. Here, we investigate the decay of female sexual traits, and the genetic causes thereof, in a transition from haplodiploid sexual reproduction to endosymbiont-induced asexual reproduction in the parasitoid wasp Asobara japonica. We take advantage of the fact that asexual females cured of their endosymbionts produce sons instead of daughters, and that these sons can be crossed with sexual females. By combining behavioral experiments with crosses designed to introgress alleles from the asexual into the sexual genome, we found that sexual attractiveness, mating, egg fertilization and plastic adjustment of offspring sex ratio (in response to variation in local mate competition) are decayed in asexual A. japonica females. Furthermore, introgression experiments revealed that the propensity for cured asexual females to produce only sons (because of decayed sexual attractiveness, mating behavior and/or egg fertilization) is likely caused by recessive genetic effects at a single locus. Recessive effects were also found to cause decay of plastic sex-ratio adjustment under variable levels of local mate competition. Our results suggest that few recessive mutations drive decay of female sexual traits, at least in asexual species deriving from haplodiploid sexual ancestors.

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“…CI is the most frequent host manipulation by Wolbachia and has thus far been reported for six insect orders (Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, and Orthoptera) and terrestrial crustaceans and mites (Ma et al 2013), while Cardinium-mediated CI has only been reported for two parasitoid wasp species (Hymenoptera), one planthopper species (Hemiptera) and a number of mite species (Hunter et al 2003;Breeuwer et al 2012;Nakamura et al 2012;Gebiola et al 2016a, b). Bacterially mediated CI is a postzygotic effect that occurs when infected males mate with uninfected females, or with females infected with bacteria that cannot rescue CI.…”

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confidence: 99%

Independent cytoplasmic incompatibility induced byCardiniumandWolbachiamaintains endosymbiont coinfections in haplodiploid thrips populations

et al. 2017

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Cardinium and Wolbachia are common maternally inherited reproductive parasites that can coinfect arthropods, yet interactions between both bacterial endosymbionts are rarely studied. For the first time, we report their independent expression of complete cytoplasmic incompatibility (CI) in a coinfected host, and CI in a species of the haplodiploid insect order Thysanoptera. In Pezothrips kellyanus, Cardinium-induced CI resulted in a combination of male development (MD) and embryonic female mortality (FM) of fertilized eggs. In contrast, Wolbachia-induced CI resulted in FM together with postembryonic mortality not previously reported as a CI outcome. Both endosymbionts appeared to not influence fecundity but virgins produced more offspring than mated females. In coinfected individuals, Wolbachia density was higher than Cardinium. Wolbachia removal did not impact Cardinium density, suggesting a lack of competition within hosts. Maternal transmission was complete for Wolbachia and high for Cardinium. Our data support theoretical predictions and empirical detection of high endosymbiont prevalence in field populations of the native range of this pest thrips. However, previous findings of more frequent loss of Wolbachia than Cardinium, particularly in field populations of the host's invasive range, suggest that genetic diversity or varying environmental factors between field populations also play a role in shaping host-endosymbiont dynamics.

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Manipulation of Arthropod Sex Determination by Endosymbionts: Diversity and Molecular Mechanisms

Cited by 51 publications

References 127 publications

Symbiont‐conferred reproduction and fitness benefits can favour their host occurrence

Symbiont‐conferred reproduction and fitness benefits can favour their host occurrence

Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality

Independent cytoplasmic incompatibility induced byCardiniumandWolbachiamaintains endosymbiont coinfections in haplodiploid thrips populations

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