Data from: Population-level consequences of complementary sex determination in a solitary parasitoid

Background: Sex determination mechanisms are known to be evolutionarily labile but the factors driving transitions in sex determination mechanisms are poorly understood. All insects of the Hymenoptera are haplodiploid, with males normally developing from unfertilized haploid eggs. Under complementary sex determination (CSD), diploid males can be produced from fertilized eggs that are homozygous at the sex locus. Diploid males have near-zero fitness and thus represent a genetic load, which is especially severe under inbreeding. Here, we study mating structure and sex determination in the parasitoid Cotesia vestalis to investigate what may have driven the evolution of two complementary sex determination loci in this species. Results: We genotyped Cotesia vestalis females collected from eight fields in four townships in Western Taiwan. 98 SNP markers were developed by aligning Illumina sequence reads of pooled DNA of eight different females against a de novo assembled genome of C. vestalis. This proved to be an efficient method for this non-model species and provides a resource for future use in related species. We found significant genetic differentiation within the sampled population but variation could not be attributed to sampling locations by AMOVA. Non-random mating was detected, with 8.1% of matings between siblings. Diploid males, detected by flow cytometry, were produced at a rate of 1.4% among diploids. Conclusions: We think that the low rate of diploid male production is best explained by a CSD system with two independent sex loci, supporting laboratory findings on the same species. Fitness costs of diploid males in C. vestalis are high because diploid males can mate with females and produce infertile triploid offspring. This severe fitness cost of diploid males combined with non-random mating may have resulted in evolution from single locus CSD to CSD with two independent loci.

背景：性别决定机制在进化过程中具有高度可塑性，但目前学界对推动其演化转变的核心驱动因素仍知之甚少。膜翅目（Hymenoptera）所有昆虫均为单倍二倍体，雄性通常由未受精的单倍体卵发育而来。在互补性别决定（complementary sex determination, CSD）机制下，若受精卵在性别位点呈纯合状态，则可发育为二倍体雄性。二倍体雄性的适合度近乎为零，因此会带来遗传负荷，且在近交情况下该负荷会显著加重。本研究以寄生性昆虫菜蛾盘绒茧蜂（Cotesia vestalis）为研究对象，探究推动该物种演化出两个互补性别决定位点的潜在因素。

结果：我们对采自中国台湾西部4个乡镇的8块农田的菜蛾盘绒茧蜂雌性个体进行了基因分型。研究人员将8只不同雌性个体的混合DNA的Illumina测序读段，比对至菜蛾盘绒茧蜂的从头组装基因组，从而开发出98个单核苷酸多态性（single nucleotide polymorphism, SNP）标记。该方法被证实对该非模式生物物种而言高效可行，同时也为后续相关物种的研究提供了可用资源。我们在采样种群中检测到显著的遗传分化，但通过分子变异方差分析（analysis of molecular variance, AMOVA）可知，该遗传变异无法通过采样地点进行解释。研究检测到非随机交配现象，其中8.1%的交配发生在同胞个体之间。通过流式细胞术检测发现，在二倍体个体中，二倍体雄性的产生比例为1.4%。

结论：我们认为，二倍体雄性的低产生率可通过具有两个独立性别位点的互补性别决定系统得到最佳解释，这一结果支持了该物种的实验室研究发现。菜蛾盘绒茧蜂的二倍体雄性存在极高的适合度成本：二倍体雄性可与雌性个体交配，但会产生不育的三倍体后代。二倍体雄性的这种严重适合度成本，结合非随机交配现象，可能推动了该物种从单一位点互补性别决定系统向两位点独立互补性别决定系统的演化。