Recurrent Losses and Rapid Evolution of the Condensin II Complex in Insects

Abstract

Condensins play a crucial role in the organization of genetic material by compacting and disentangling chromosomes. Based on studies in a few model organisms, the condensins I and II complexes are considered to have distinct functions, with the condensin II complex playing a role in meiosis and somatic pairing of homologous chromosomes in Drosophila. Intriguingly, the Cap-G2 subunit of condensin II is absent in Drosophila melanogaster, and this loss may be related to the high levels of chromosome pairing seen in flies. Here, we find that all three non-SMC subunits of condensin II (Cap-G2, Cap-D3, and Cap-H2) have been repeatedly and independently lost in taxa representing multiple insect orders, with some taxa lacking all three. We also find that all non-Dipteran insects display near-uniform low-pairing levels regardless of their condensin II complex composition, suggesting that some key aspects of genome organization are robust to condensin II subunit losses. Finally, we observe consistent signatures of positive selection in condensin subunits across flies and mammals. These findings suggest that these ancient complexes are far more evolutionarily labile than previously suspected, and are at the crossroads of several forms of genomic conflicts. Our results raise fundamental questions about the specific functions of the two condensin complexes in taxa that have experienced subunit losses, and open the door to further investigations to elucidate the diversity of molecular mechanisms that underlie genome organization across various life forms.

Keywords: chromosome pairing; condensin; molecular evolution.

Fig. 1.

Insect phylogeny shows evidence for multiple independent losses of condensin II subunits. Based on genome sequence analysis, non-SMC subunits have been repeatedly lost in different combinations across several insect orders. Phylogeny is based on Misof et al. (2014) Bold names represent orders containing species where interphase chromosome pairing was also assessed. Condensin II subunits displayed for each order represent all subunits detected in any member of the order; some subgroups within the order have lost further subunits. In all species sampled, we were able to identify all condensin I-specific subunits. This cladogram shows phylogenetic relationships only, and branch lengths do not represent divergence time. For an insect phylogeny with branch lengths to scale and estimates of divergence time provided, see Misof et al. (2014).

Fig. 2.

No relationship between condensin II composition and homolog pairing. Species missing more condensin II subunits do not tend to have higher pairing rates as measured by Oligopaint DNA-FISH. Blue bars represent the proportion of nuclei in each species displaying a single FISH signal. Values for each species represent the observed pairing proportion and number of nuclei scored. Each set of values represents results from a single Oligopaint probe. Error bars show 95% confidence intervals (binomial proportion with Wilson score). Circles below species names correspond to condensin II complex composition. Cladogram of insect species, based on the phylogeny of Misof et al. (2014), shows relationships only and is not to scale.

Fig. 3.

Recurrent positive selection in cohesin and condensin subunits in flies. Results of PAML show widespread positive selection in condensin and cohesin subunits among Drosophila species. P-values for PAML are derived from a log-ratio test using the log-likelihood scores for the positive selection and neutral models. Using the Bonferroni correction to account for multiple testing, bold values represent statistically significant results with a threshold of P = 0.00417.

Fig. 4.

PAML analyses reveal signatures of positive selection in condensins and cohesin in mammal clades. P-values are derived from a log-ratio test using the log-likelihood scores for the positive selection and neutral models. Using the Bonferroni correction to account for multiple testing, bold values represent statistically significant results with a threshold of P = 0.00417.