Comparative Transcriptomics across Nematode Life Cycles Reveal Gene Expression Conservation and Correlated Evolution in Adjacent Developmental Stages

Abstract

Nematodes are highly abundant animals with diverse habitats and lifestyles. Some are free living whereas others parasitize animals or plants, and among the latter, infection abilities change across developmental stages to infect hosts and complete life cycles. To determine the relationship between transcriptome evolution and morphological divergences among nematodes, we compared 48 transcriptomes of different developmental stages across eight nematode species. The transcriptomes were clustered broadly into embryo, larva, and adult stages, with the developmental plastic stages were separated from common larval stages within the larval branch. This suggests that development was the major determining factor after lifestyle changes, such as parasitism, during transcriptome evolution. Such patterns were partly accounted for by tissue-specific genes—such as those in oocytes and the hypodermis—being expressed at different proportions. Although nematodes typically have 3–5 larval stages, the transcriptomes for these stages were found to be highly correlated within each species, suggesting high similarity among larval stages across species. For the Caenorhabditis elegans–Caenorhabditis briggsae and Strongyloides stercoralis–Strongyloides venezuelensis comparisons, we found that ∼50% of genes were expressed at multiple stages, whereas half of their orthologs were also expressed in multiple but different stages. Such frequent changes in expression have resulted in concerted transcriptome evolution across adjacent stages, thus generating species-specific transcriptomes over the course of nematode evolution. Our study provides a first insight into the evolution of nematode transcriptomes beyond embryonic development.