The Same or Not the Same: Lineage-Specific Gene Expansions and Homology Relationships in Multigene Families in Nematodes

Homology is a fundamental concept in comparative biology and a crucial tool for the analysis of character distribution. Introduced by Owen in 1843 (Lectures on comparative anatomy and physiology of the invertebrate animals, Longman, Brown, Green and Longman, London) in a morphological context, homology can similarly be applied to protein-coding genes. However, in molecular biology the proper distinction between orthology and paralogy was long limited by the absence of whole-genome sequencing data. By now, genome-wide sequencing allows comprehensive analyses of the homology of genes and gene families at the level of an entire phylum. Here, we analyze a manually curated dataset of more than 2,000 proteins from the genomes of 11 nematode species of seven different genera, including free-living and animal and plant parasites to study the principles of homology assignments in gene families. Using all sequenced species as an extensive outgroup, we specifically focus on the two model species Caenorhabditis elegans and Pristionchus pacificus and compare enzymes involved in detoxification of xenobiotics and synthesis of fatty acids. We find that only a small proportion of genes in these families are one-to-one orthologs and that their history is shaped by massive duplication events. Of a total of 349 and 528 genes from C. elegans and P. pacificus, respectively, only 39 are one-to-one orthologs. Thus, frequent amplifications and losses are a widespread phenomenon in nematode lineages. We also report variation in birth and death rates depending on gene families and nematode lineages. Finally, we discuss the consequence of the near absence of one-to-one orthology in related organisms for the application of the homology concept to protein-coding genes in the era of whole-genome sequencing data