Consequences of Asexuality in Natural Populations: Insights from Stick Insects

Abstract

Recombination is a fundamental process with significant impacts on genome evolution. Predicted consequences of the loss of recombination include a reduced effectiveness of selection, changes in the amount of neutral polymorphisms segregating in populations, and an arrest of GC-biased gene conversion. Although these consequences are empirically well documented for nonrecombining genome portions, it remains largely unknown if they extend to the whole genome scale in asexual organisms. We identify the consequences of asexuality using de novo transcriptomes of five independently derived, obligately asexual lineages of stick insects, and their sexual sister-species. We find strong evidence for higher rates of deleterious mutation accumulation, lower levels of segregating polymorphisms and arrested GC-biased gene conversion in asexuals as compared with sexuals. Taken together, our study conclusively shows that predicted consequences of genome evolution under asexuality can indeed be found in natural populations.

Fig. 1.

Phylogeny of Timema species (sexual species phylogeny redrawn from Riesch et al. 2017; asexual lineages added from Schwander et al. 2011). Sexual species are colored red, asexual species blue. For this study, five sex–asex species pairs were used (for Timema douglasi only the southern lineage).

Fig. 2.

Asexual lineages ranked from youngest to oldest as estimated from Jukes–Cantor corrected divergence between sexual–asexual sister-species (depending on the species pair, using 5,329–5,908 pairwise orthologs). Tte: Timema tahoe, Tms: Timema monikensis, Tdi: Timema douglasi, Tsi: Timema shepardi, Tge: Timema genevievae. The oldest asexual lineage Timema genevievae, was previously estimated to be ∼1.5 My old (Schwander et al. 2011).

Fig. 3.

Mean GC3 content (with 95% CI) and GC3 standard deviation of the 3,010 ten-species orthologs of sexual (in red) and asexual (in blue) Timema species. Tbi: T. bartmani, Tte: T. tahoe, Tce: T. cristinae, Tms: T. monikensis, Tps: T. poppensis, Tdi: T. douglasi, Tcm: T. californicum, Tsi: T. shepardi, Tpa: T. podura, Tge: T. genevievae.

Fig. 4.

Medians (and 95% CI with 5,000 bootstrap replicates) of (A) number of transcripts containing SNPs and (B) proportion of variable sites per transcript for sexual (red) and asexual (blue) Timema species.

Fig. 5.

Means (and 95% CI) of nonsynonymous segregating polymorphisms (pN/pS) of sexual (in red) and asexual (in blue) Timema species. Tbi: T. bartmani, Tte: T. tahoe, Tce: T. cristinae, Tms: T. monikensis, Tps: T. poppensis, Tdi: T. douglasi, Tcm: T. californicum, Tsi: T. shepardi, Tpa: T. podura, Tge: T. genevievae. Species pairs are ranked by age of the asexual lineage (youngest to oldest).

Fig. 6.

Means (and 95% CI) of ω = dN/dS ratios from 2,487 orthologs in sexual (in red) and asexual (in blue) Timema species. Tbi: T. bartmani, Tte: T. tahoe, Tce: T. cristinae, Tms: T. monikensis, Tps: T. poppensis, Tdi: T. douglasi, Tcm: T. californicum, Tsi: T. shepardi, Tpa: T. podura, Tge: T. genevievae. Species pairs are ranked by age of the asexual lineage (youngest to oldest).

Fig. 7.

Means (and 95% CI) of the codon deviation coefficient (CDC) of sexual (in red) and asexual (in blue) Timema species. Tbi: T. bartmani, Tte: T. tahoe, Tce: T. cristinae, Tms: T. monikensis, Tps: T. poppensis, Tdi: T. douglasi, Tcm: T. californicum, Tsi: T. shepardi, Tpa: T. podura, Tge: T. genevievae. Species pairs are ranked by age of the asexual lineage (youngest to oldest).