Genetic incompatibility drives mate choice in a parasitic wasp

Thiel, Andra; Weeda, Anne C.; Boer, Jetske G. de; Hoffmeister, Thomas S.

doi:10.1186/1742-9994-10-43

Cited by 15 publications

(19 citation statements)

References 29 publications

(30 reference statements)

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“…The apparent preference in wasps to place male eggs could reflect inbreeding avoidance and/or a mechanism to reduced diploid male production. In some hymenopteran species with CSD, females will avoid mating with males that are genetically similar at the sex determination locus (Harper, Bagley, Thompson, & Linnen, ; Metzger, Bernstein, Hoffmeister, & Desouhant, ; Ruf, Dorn, & Mazzi, ; Thiel, Weeda, De Boer, & Hoffmeister, ). Consequently, premating mechanisms linked to low diversity (e.g., avoidance of genetically similar mates) could also explain the higher than expected frequency of unmated females.…”

Section: Discussionmentioning

confidence: 99%

Mechanisms that influence sex ratio variation in the invasive hymenopteran Sirex noctilio in South Africa

Queffelec

Wooding

Greeff

et al. 2019

Ecology and Evolution

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Sirex noctilio is an economically important invasive pest of commercial pine forestry in the Southern Hemisphere. Newly established invasive populations of this woodwasp are characterized by highly male‐biased sex ratios that subsequently revert to those seen in the native range. This trend was not observed in the population of S. noctilio from the summer rainfall regions in South Africa, which remained highly male‐biased for almost a decade. The aim of this study was to determine the cause of this persistent male bias. As an explanation for this pattern, we test hypotheses related to mating success, female investment in male versus female offspring, and genetic diversity affecting diploid male production due to complementary sex determination. We found that 61% of females in a newly established S. noctilio population were mated. Microsatellite data analysis showed that populations of S. noctilio from the summer rainfall regions in South Africa are far less genetically diverse than those from the winter rainfall region, with mean Nei's unbiased gene diversity indexes of 0.056 and 0.273, respectively. These data also identified diploid males at low frequencies in both the winter (5%) and summer (2%) rainfall regions. The results suggest the presence of a complementary sex determination mechanism in S. noctilio , but imply that reduced genetic diversity is not the main driver of the male bias observed in the summer rainfall region. Among all the factors considered, selective investment in sons appears to have the most significant influence on male bias in S. noctilio populations. Why this investment remains different in frontier or early invasive populations is not clear but could be influenced by females laying unfertilized eggs to avoid diploid male production in populations with a high genetic relatedness.

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Section: Discussionmentioning

confidence: 99%

Mechanisms that influence sex ratio variation in the invasive hymenopteran Sirex noctilio in South Africa

Queffelec

Wooding

Greeff

et al. 2019

Ecology and Evolution

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“…Laboratory studies in Bracon brevicornis have reported an avoidance of mating with a partner harboring the same allele at the sl‐CSD locus (i.e., avoidance of matched matings; Thiel et al. ), and sib‐mating avoidance was observed in V. canescens (Metzger et al. ).…”

Section: Discussionmentioning

confidence: 99%

“…On the contrary, the lack of mate discrimination in C. rubecula could explain the relatively high DMP observed in its field populations (de Boer et al 2012). Laboratory studies in Bracon brevicornis have reported an avoidance of mating with a partner harboring the same allele at the sl-CSD locus (i.e., avoidance of matched matings; Thiel et al 2013), and sib-mating avoidance was observed in V. canescens (Metzger et al 2010a). Such behaviors should reduce the DMP and thus lessens the production of unfit offspring (Parker 1983;Chuine et al 2015).…”

Section: Discussionmentioning

confidence: 99%

“…Some Hymenoptera with sl-CSD have undifferentiated populations beyond a 100-km scale (Estoup et al 1996;Zimmermann et al 2011), suggesting high dispersal abilities. Mate choice can also influence the production of diploid males with a reduction expected in case of inbreeding avoidance (Whitehorn et al 2009;Metzger et al 2010a;Thiel et al 2013). Such behaviors may mitigate the diploid male vortex (Hein et al 2009).…”

Section: Introductionmentioning

confidence: 99%

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Diploid male production correlates with genetic diversity in the parasitoid wasp Venturia canescens: a genetic approach with new microsatellite markers

Collet

Vayssade

Auguste

et al. 2016

Ecology and Evolution

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Sex determination is ruled by haplodiploidy in Hymenoptera, with haploid males arising from unfertilized eggs and diploid females from fertilized eggs. However, diploid males with null fitness are produced under complementary sex determination (CSD), when individuals are homozygous for this locus. Diploid males are expected to be more frequent in genetically eroded populations (such as islands and captive populations), as genetic diversity at the csd locus should be low. However, only a few studies have focused on the relation between population size, genetic diversity, and the proportion of diploid males in the field. Here, we developed new microsatellite markers in order to assess and compare genetic diversity and diploid male proportion (DMP) in populations from three distinct habitat types – mainland, island, or captive –, in the parasitoid wasp Venturia canescens. Eroded genetic diversity and higher DMP were found in island and captive populations, and habitat type had large effect on genetic diversity. Therefore, DMP reflects the decreasing genetic diversity in small and isolated populations. Thus, Hymenopteran populations can be at high extinction risk due to habitat destruction or fragmentation.

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“…Moreover, many species of Hymenoptera have life histories that could accelerate this extinction vortex by increasing the probability of producing diploid males and of females mating with them. For instance, gregarious immature development may increase the probability of sib‐mating, and viability of diploid males along with monandry may lower the fitness of sib‐mated females as well as females mating with diploid males (Godfray, ; Thiel & Weeda, ; Thiel, Weeda, de Boer, & Hoffmeister, ; Zayed & Packer, ). This puts strong pressure on Hymenoptera with CSD to develop ways to decrease sib‐mating, for example, through behavioral mechanisms (Metzger, Bernstein, Hoffmeister, & Desouhant, ; Ode, Antolin, & Strand, ; Van Wilgenburg, Driessen, & Beukeboom, ).…”

Section: Introductionmentioning

confidence: 99%

Effects of inbreeding on a gregarious parasitoid wasp with complementary sex determination

Zaviezo

Retamal

Urvois

et al. 2017

Evolutionary Applications

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Inbreeding and inbreeding depression are processes in small populations of particular interest for a range of human activities such as animal breeding, species conservation, or pest management. In particular, biological control programs should benefit from a thorough understanding of the causes and consequences of inbreeding because natural enemies experience repetitive bottlenecks during importation, laboratory rearing, and introduction. Predicting the effect of inbreeding in hymenopteran parasitoid wasps, frequently used in biological control programs, is nonetheless a difficult endeavor. In haplodiploid parasitoids, the purge of deleterious alleles via haploid males should reduce genetic load, but if these species also have complementary sex determination (CSD), abnormal diploid males will be produced, which may jeopardize the success of biological control introductions. Mastrus ridens is such a parasitoid wasp with CSD, introduced to control the codling moth, Cydia pomonella (L.). We studied its life history traits in the laboratory under two conditions: inbred (full‐sib) and outbred (nonsib) crosses, across five generations, to examine the consequences of inbreeding in this species. We found that in inbred lines, nonreproducing females live less, the number of daughters produced was lower, and sex ratio (proportion of males) and proportion of diploid males were higher. Diploid males were able to produce fertile daughters, but fewer than haploid males. Lineage survival was similar for inbred and outbred lines across the five generations. The most significant decrease in fitness was thus a consequence of the production of diploid males, but this effect was not as extreme as in most other species with CSD, due to the fertility of diploid males. This study highlights the importance of determining the type of sex determination in parasitoid wasps used for biological control, and the importance of maintaining genetic diversity in species with CSD when importation or augmentation is the goal.

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Genetic incompatibility drives mate choice in a parasitic wasp

Cited by 15 publications

References 29 publications

Mechanisms that influence sex ratio variation in the invasive hymenopteran Sirex noctilio in South Africa

Mechanisms that influence sex ratio variation in the invasive hymenopteran Sirex noctilio in South Africa

Diploid male production correlates with genetic diversity in the parasitoid wasp Venturia canescens: a genetic approach with new microsatellite markers

Effects of inbreeding on a gregarious parasitoid wasp with complementary sex determination

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