Chromosome-level genome assemblies of two hemichordates provide new insights into deuterostome origin and chromosome evolution

Abstract

Deuterostomes are an animal superphylum that includes Hemichordata and Echinodermata (together Ambulacraria) and Chordata. The diversity of deuterostome body plans has made it challenging to reconstruct their ancestral condition and to decipher the genetic changes that drove the diversification of deuterostome lineages. Here, we generate chromosome-level genome assemblies of two hemichordate species,Ptychodera flavaandSchizocardium californicum, and use comparative genomic approaches to infer the chromosomal architecture of the deuterostome common ancestor and delineate lineage-specific chromosomal modifications. We show that hemichordate chromosomes (1N=23) exhibit remarkable chromosome-scale macrosynteny when compared to other deuterostomes, and can be derived from 24 deuterostome ancestral linkage groups (ALGs). These deuterostome ALGs in turn match previously inferred bilaterian ALGs, consistent with a relatively short transition from the last common bilaterian ancestor to the origin of deuterostomes. Based on this deuterostome ALG complement, we deduced chromosomal rearrangement events that occurred in different lineages. For example, a fusion-with-mixing event produced an Ambulacraria-specific ALG that subsequently split into two chromosomes in extant hemichordates, while this homologous ALG further fused with another chromosome in sea urchins. Orthologous genes distributed in these rearranged chromosomes are enriched for functions in various developmental processes. We found that the deeply conserved Hox clusters are located in highly rearranged chromosomes but have lower densities of transposable elements within the clusters. We also provide evidence that the deuterostome-specific pharyngeal gene cluster was established via the combination of three pre-assembled microsyntenic blocks. We suggest that since chromosomal rearrangement events and formation of new gene clusters may change the regulatory controls of developmental genes, these events may have contributed to the evolution of diverse body plans among deuterostomes.

Annelid comparative genomics and the evolution of massive lineage-specific genome rearrangement in bilaterians

“…These structural alterations play pivotal roles in fundamental biological phenomena, including recombination (Rieseberg 2001;Näsvall et al 2023;Yoshida et al 2023), adaptation (Dunham et al 2002;Coyle and Kroll 2007;Lowry and Willis 2010;Jones et al 2012;Wellenreuther and Bernatchez 2018), speciation (Noor et al 2001;de Vos et al 2020;Augustijnen et al 2024), disease (Lupski and Stankiewicz 2005), and ultimately, the emergence of novel phenotypic traits. While some lineages exhibit remarkable conservation of genome structure over extended evolutionary timescales, others display striking divergence, with chromosomes rearranged in unpredictable patterns (Wang et al 2017;Simakov et al 2022;Ivankovic et al 2023;Lin et al 2023;Martín-Zamora et al 2023). Unraveling the evolutionary forces driving such lineage-specific scrambling of gene sets can provide valuable insights into the process of adaptation and the evolution of animal diversity.…”

“…This conserved gene linkage, or macrosynteny, can be used to track orthologous chromosomes across highly divergent species and is emerging as a powerful tool for studying genome rearrangements. This technique has thus far largely been applied to long-range comparisons across metazoans (Simakov et al 2013;Simakov et al 2022;Lin et al 2023;Schultz et al 2023;Zimmermann et al 2023) or to compare very closely related species, for example Acropora corals (Locatelli et al 2023) or cryptic species of the tunicate Oikopleura dioica (Plessy et al 2024). Such studies have been highly fruitful, elucidating the genome structure of the last common ancestor of bilaterians (Putnam et al 2007;Putnam et al 2008;Simakov et al 2022;Marlétaz et al 2023) and developing algorithms for inferring rearrangement history (Ferretti et al 1996;DasGupta et al 1997;Mackintosh et al 2023).…”