Convergent consequences of parthenogenesis on stick insect genomes

Abstract

The shift from sexual reproduction to parthenogenesis has occurred repeatedly in animals, but how the loss of sex affects genome evolution remains poorly understood. We generated de novo reference genomes for five independently evolved parthenogenetic species in the stick insect genus Timema and their closest sexual relatives. Using these references in combination with population genomic data, we show that parthenogenesis results in an extreme reduction of heterozygosity, and often leads to genetically uniform populations. We also find evidence for less effective positive selection in parthenogenetic species, supporting the view that sex is ubiquitous in natural populations because it facilitates fast rates of adaptation. Contrary to studies of non-recombining genome portions in sexual species, genomes of parthenogenetic species do not accumulate transposable elements (TEs), likely because successful parthenogens derive from sexual ancestors with inactive TEs. Because we are able to conduct replicated comparisons across five species pairs, our study reveals, for the first time, how animal genomes evolve in the absence of sex in natural populations, providing empirical support for the negative consequences of parthenogenetic reproduction as predicted by theory.

Dynamics of sex-biased gene expression during development in the stick insectTimema californicum

“…(11 F-biased and M-biased) genes for which a previous study (Jaron et al, 2020) detected signatures of positive selection. Excluding these 19 genes did not change our results (Supplemental Table 7a).…”

“…To calculate sequence divergence rates, we used the 7098 one-to-one orthologs between T. californicum and T. poppensis from (Jaron et al, 2020). Coding sequences were codon-aligned using prank v.170427 (Loytynoja, 2014).…”

“…Sequence divergence rates were obtained for 14 out of 26 SBG at the hatchling stage, 323/568 at the juvenile stage, and 1286/2485 at the adult stage. To account for the influence of positive selection we repeated our analyses after removing genes with evidence for positive selection in the T. californicum lineage (identified in (Jaron et al, 2020)).…”

“…Elevated rates of sequence evolution are likely the result of reduced purifying selection, but stronger positive selection may also contribute to fast sequence evolution in some genes. To test this possibility, we repeated our analysis after excluding 19 (11 F-biased and 8 M-biased) genes for which a previous study (Jaron et al 2020) detected signatures of positive selection.…”

“…Sex-biased genes at the hatchling stage are particularly interesting because they reveal sexual differentiation prior to visible morphological differences. We therefore looked for functional annotations of the 26 sex-biased genes at the hatchling stage in the T. californicum reference genome from (Jaron et al, 2020). However, only 16 out of the 26 sex-biased genes had functional annotations and only one (vitellogenin receptor) had a clear link to sexual differentiation (Figure 3b).…”