From solitary to colonial with zooid miniaturization: ancestral-state reconstruction based on NGS data of stolidobranch ascidians

Abstract

The size of organisms has consistently intrigued researchers across various disciplines in biology. However, the evolutionary process of zooid miniaturization in colonial animals remained an enigmatic topic. The family Styelidae, within the ascidian order Stolidobranchia, showcases a diverse spectrum of coloniality, positioning it as an ideal candidate for delving into the intricacies of colonial evolution. In this research, we inferred a phylogenomic relationship mainly within Styelidae using transcriptomes of a total of 42 ascidians; from 17 species sampled in Israel and Japan and transcriptome data from 25 species sourced from a previous study and a database. Through ancestral-state reconstruction, our analysis indicated a clear directional change: following the acquisition of coloniality, zooids tended to become progressively smaller. This miniaturization is likely an adaptive response, enabling organisms to swiftly colonize limited marine substrate. We formulated a mathematical model suggesting that zooid miniaturization, due to living space constraints, would result in a faster asexual cycle and accelerated expansion in a colony. Our data also suggested that coloniality evolved independently three times within Styelidae. Moreover, once colonial traits are established, they appear to be consistently preserved, underscoring their biological importance in the colonial lineage.