Parallel evolution of X chromosome-specific SMC complexes in two nematode lineages [ChIP-Seq]

Mechanisms of X chromosome dosage compensation have been studied in model organisms with distinct sex chromosome ancestry. However, the diversity of mechanisms as a function of sex chromosome evolution is largely unknown. Here, we anchor ourselves to the nematode Caenorhabditis elegans, where dosage compensation is accomplished by an X chromosome specific condensin that belongs to the family of structural maintenance of chromosomes (SMC) complexes. By combining a phylogenetic analyses of the C. elegans dosage compensation complex with a comparative analysis of its epigenetic signatures, such as X-specific topologically associating domains (TADs) and enrichment of H4K20me1, we show that the condensin-mediated mechanism evolved recently in the lineage leading to Caenorhabditis following an SMC-4 duplication. Unexpectedly, we found an independent duplication of SMC-4 in Pristionchus pacificus along with X-specific TADs and H4K20me1 enrichment, which suggests that condensin-mediated dosage compensation evolved more than once in nematodes. Differential expression analysis between sexes in several nematode species indicates that dosage compensation itself precedes the evolution of X-specific condensins. In Rhabditina, X-specific condensins may have evolved in the presence of an existing mechanism linked to H4K20 methylation as Oscheius tipulae X chromosomes are enriched for H4K20me1 without SMC-4 duplication or TADs. In contrast, Steinernema hermaphroditum lacks H4K20me1 enrichment, SMC-4 duplication, and TADs. Together, our results indicate that dosage compensation mechanisms continue to evolve in species with shared X chromosome ancestry, and SMC complexes may have been co-opted at least twice in nematodes, suggesting that the process of evolving chromosome wide gene regulatory mechanisms are constrained. ChIP-seq for histone modifications H4K20me1 and H3K4me3, as well as IgG in the nematodes Steinernema hermaphroditum, Pristionchus pacificus, and Oscheius tipulae Please note that the records have been updated on Aug 4, 2025 with the additional samples and revised protocol description.