Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis

Boer, Jetske G. de; Ode, Paul J.; Vet, Louise E. M.; Whitfield, James B.; Heimpel, George E.

doi:10.1038/sj.hdy.6800995

Cited by 64 publications

(71 citation statements)

References 52 publications

(65 reference statements)

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“…Because of the complementary sex-determination (csd) system of Hymenoptera, homozygous individuals at the sex-determining loci develop into diploid males (Cook and Crozier, 1995). Diploid males constitute particularly high fitness costs to colonies since they are usually sterile or they father a sterile, triploid female progeny (de Boer et al, 2007;Cournault et al, 2006;Krieger et al, 1999;Liebert et al, 2004). Whether diploid males always produce diploid spermatozoa, or not, remains unclear; FCM could greatly help in this respect.…”

Section: Discussionmentioning

confidence: 99%

Rapid determination of sperm number in ant queens by flow cytometry

Cournault

Aron

2008

Insect. Soc.

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Abstract. In social Hymenoptera, queens receive a given amount of sperm during a single or multiple inseminations once and for all. The amount of sperm stored at mating determines the maximum number of fertilized eggs queens can produce for the rest of their reproductive life. We propose flow cytometry (FCM) as a method to estimate the concentration of sperm cells, as well as their ploidy level, in queens spermathecae. Our data, obtained from 5 ant species, show that FCM is precise, repeatable, easy to conduct and rapid. Estimates of variation of spermathecal content always remain below 10 %, and samples can be analysed in less than 5 minutes. Flow cytometry appears as an excellent method for comparative analyses of sperm number within and between ant species.

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Section: Discussionmentioning

confidence: 99%

Rapid determination of sperm number in ant queens by flow cytometry

Cournault

Aron

2008

Insect. Soc.

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“…One to 4 replicates were done per original mother-son mating for a total of 22-26 replicates in each generation. We ensured using haploid males in each cross by allowing virgin females to oviposit in 10-15 second and third instar diamondback moth larvae before mating and using these male offspring in brother-sister matings of the next generation (de Boer et al 2007b). To allow mating, pairs were kept together for 24 hr in a plastic vial (2.5 cm diameter, 6.5 cm high) with a piece of host-damaged cabbage leaf and a droplet of honey.…”

Section: Methodsmentioning

confidence: 99%

“…Flow cytometry: Ploidy of male offspring of replicates that produced at least one female was identified with flow cytometry, following methods described by de Boer et al (2007b). In short, the head of an individual wasp was pulverized in Galbraith buffer (Galbraith et al 1983) and DNA was stained with propidium iodide.…”

Section: Methodsmentioning

confidence: 99%

“…Under single-locus (sl)-CSD, female development is initiated by heterozygosity at a single, highly polymorphic, sex locus. Homozygotes at the sex locus develop into inviable or sterile diploid males (Whiting 1943;Cook 1993b;Cook and Crozier 1995;Holloway et al 1999;de Boer et al 2007b), with the exception of the vespid wasp Euodynerus foraminatus, in which diploid males have near normal fertility (Cowan and Stahlhut 2004). The production of diploid males increases dramatically under conditions of inbreeding or low genetic diversity and represents a severe genetic load.…”

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confidence: 99%

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Experimental Support for Multiple-Locus Complementary Sex Determination in the Parasitoid Cotesia vestalis

et al. 2008

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Despite its fundamental role in development, sex determination is highly diverse among animals. Approximately 20% of all animals are haplodiploid, with haploid males and diploid females. Haplodiploid species exhibit diverse but poorly understood mechanisms of sex determination. Some hymenopteran insect species exhibit single-locus complementary sex determination (sl-CSD), where heterozygosity at a polymorphic sex locus initiates female development. Diploid males are homozygous at the sex locus and represent a genetic load because they are inviable or sterile. Inbreeding depression associated with CSD is therefore expected to select for other modes of sex determination resulting in fewer or no diploid males. Here, we investigate an alternative, heretofore hypothetical, mode of sex determination: multiple-locus CSD (ml-CSD). Under ml-CSD, diploid males are predicted to develop only from zygotes that are homozygous at all sex loci. We show that inbreeding for eight generations in the parasitoid wasp Cotesia vestalis leads to increasing proportions of diploid males, a pattern that is consistent with ml-CSD but not sl-CSD. The proportion of diploid males (0.27 6 0.036) produced in the first generation of inbreeding (mother-son cross) suggests that two loci are likely involved. We also modeled diploid male production under CSD with three linked loci. Our data visually resemble CSD with linked loci because diploid male production in the second generation was lower than that in the first. To our knowledge, our data provide the first experimental support for ml-CSD.

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“…First, in all but one studied species [5], diploid males are inviable or sterile [6][7][8][9], the latter associated with underdeveloped testes and/or production of diploid sperm [10][11][12][13][14][15]. Second, studies in ants showed that diploid males are usually larger than their normal haploid counterparts [8,16].…”

Section: Introductionmentioning

confidence: 99%

Effects of ploidy and sex-locus genotype on gene expression patterns in the fire antSolenopsis invicta

et al. 2014

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Males in many animal species differ greatly from females in morphology, physiology and behaviour. Ants, bees and wasps have a haplodiploid mechanism of sex determination whereby unfertilized eggs become males while fertilized eggs become females. However, many species also have a low frequency of diploid males, which are thought to develop from diploid eggs when individuals are homozygous at one or more sex determination loci. Diploid males are morphologically similar to haploids, though often larger and typically sterile. To determine how ploidy level and sex-locus genotype affect gene expression during development, we compared expression patterns between diploid males, haploid males and females (queens) at three developmental timepoints in Solenopsis invicta. In pupae, gene expression profiles of diploid males were very different from those of haploid males but nearly identical to those of queens. An unexpected shift in expression patterns emerged soon after adult eclosion, with diploid male patterns diverging from those of queens to resemble those of haploid males, a pattern retained in older adults. The finding that ploidy level effects on early gene expression override sex effects (including genes implicated in sperm production and pheromone production/perception) may explain diploid male sterility and lack of worker discrimination against them during development.

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Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis

Cited by 64 publications

References 52 publications

Rapid determination of sperm number in ant queens by flow cytometry

Rapid determination of sperm number in ant queens by flow cytometry

Experimental Support for Multiple-Locus Complementary Sex Determination in the Parasitoid Cotesia vestalis

Effects of ploidy and sex-locus genotype on gene expression patterns in the fire antSolenopsis invicta

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