Sex determination meltdown upon biological control introduction of the parasitoid Cotesia rubecula?

Abstract

Natural enemies may go through genetic bottlenecks during the process of biological control introductions. Such bottlenecks are expected to be particularly detrimental in parasitoid Hymenoptera that exhibit complementary sex determination (CSD). CSD is associated with a severe form of inbreeding depression because homozygosity at one or multiple sex loci leads to the production of diploid males that are typically unviable or sterile. We observed that diploid males occur at a relatively high rate (8-13% of diploid adults) in a field population of Cotesia rubecula in Minnesota, USA, where this parasitoid was introduced for biological control of the cabbage white Pieris rapae. However, our laboratory crosses suggest two-locus CSD in a native Dutch population of C. rubecula and moderately high diploid males survival (approximately 70%), a scenario expected to produce low proportions of diploid males. We also show that courtship behavior of diploid males is similar to that of haploid males, but females mated to diploid males produce only very few daughters that are triploid. We use our laboratory data to estimate sex allele diversity in the field population of C. rubecula and discuss the possibility of a sex determination meltdown from two-locus CSD to effective single-locus CSD during or after introduction.

Keywords: Pieris rapae; cabbage; complementary sex determination; diploid males; haplodiploidy; life history; natural enemies; parasitic wasps.

Figure 1

Box plots of diploid male proportion (A), sex ratio (B), diploid family size (C) and number of females, haploid and diploid males normalized per 100 hosts (D) in three types of crosses: mother–son crosses (left), brother–sister crosses (middle) and control crosses (right). Panels (A) and (B) include boxplots of 50 000 simulations for three combinations of parameter values of the number of complementary sex determination (CSD) loci (n _loci) and the probability of diploid male survival (s) that gave the highest likelihood for single-locus CSD, two-locus CSD and three-locus CSD (Fig. S2). In panels (A), (B) and (C), boxes represent 0.25 and 0.75 quantiles and median value, whiskers represent 0.025 and 0.975 quantiles and outliers are shown as black bullets. In panel (D), error bars represent standard errors.