Cnidaria (sea anemones, jellyfish, corals and hydra) form a close sister group to Bilateria. Within this clade, the sea anemone Nematostella vectensis has emerged as a slow evolving model for investigating characteristics of the cnidarian-bilaterian common ancestor, which diverged near the Cambrian explosion. Here, using long read sequencing and high throughput chromosome conformation capture, we generate high quality chromosome-level genome assemblies for N. vectensis and the closely related edwardsiid sea anemone, Scolanthus callimorphus. In both cases we find a robust set of 15 chromosomes comprising a stable linkage group detectable within all major clades of sequenced cnidarian genomes. Further, both genomes show remarkable chromosomal conservation with chordates. In contrast with Bilateria, we report that extended Hox and NK gene clusters are chromosomally linked but do not retain a tight spatial conservation. Accordingly, there is a lack of evidence for topologically associated domains, which have been implicated in the evolutionary pressure to retain tight microsyntenic gene clusters. We also uncover ultra-conserved noncoding elements at levels previously undetected in non-chordate lineages. Both genomes are accessible through an actively updated genome browser and database at https://simrbase.stowers.org

Understanding how organisms adapt to the environment is a major goal of modern biology. Parallel evolution—the independent evolution of similar phenotypes in different populations—provides a powerful framework to investigate the evolutionary potential of populations, the constraints of evolution, its repeatability and therefore its predictability. Here, we quantified the degree of gene expression and functional parallelism across replicated ecotype formation in Heliosperma pusillum (Caryophyllaceae), and gained insights into the architecture of adaptive traits. Population structure analyses and demographic modelling support a previously formulated hypothesis of parallel polytopic divergence of montane and alpine ecotypes. We detect a large proportion of differentially expressed genes (DEGs) underlying divergence within each replicate ecotype pair, with a strikingly low number of shared DEGs across pairs. Functional enrichment of DEGs reveals that the traits affected by significant expression divergence are largely consistent across ecotype pairs, in strong contrast to the nonshared genetic basis. The remarkable redundancy of differential gene expression indicates a polygenic architecture for the diverged adaptive traits. We conclude that polygenic traits appear key to opening multiple routes for adaptation, widening the adaptive potential of organisms.

Understanding how organisms adapt to the environment is a major goal of modern biology. Parallel evolution - the independent evolution of similar phenotypes in different populations - provides a powerful framework to explore this question. Here, we quantified the degree of gene expression and functional parallelism across replicated ecotype formation in Heliosperma pusillum (Caryophyllaceae) and gained insights into the architecture of adaptive traits. Population structure analyses and demographic modelling confirm the previously formulated hypothesis of parallel polytopic divergence of montane and alpine ecotypes. We detect a large proportion of differentially expressed genes (DEGs) underlying adaptation of each replicate ecotype pair, with a strikingly low amount of shared DEGs across pairs. Functional enrichment of DEGs reveals that the traits affected by divergent gene expression are the same across ecotype pairs, in strong contrast to the non-shared genetic basis. The remarkable redundancy of differential gene expression indicates that diverged adaptive traits are highly polygenic. We conclude that polygenic traits appear key to opening multiple routes for adaptation, widening the adaptive potential of organisms.

Draft genome sequences of non-bilaterian species have provided important insights into the evolution of the metazoan gene repertoire. However, there is little information about the evolution of gene clusters, genome architectures and karyotypes during animal evolution. Here we report chromosome-level genome assemblies of two related anthozoan cnidarians, the sea anemones, Nematostella vectensis and Scolanthus callimorphus. We find a robust set of 15 chromosomes with a clear one-to-one correspondence of the chromosomes between the two species. We show that, in contrast to Bilateria, Hox and NK clusters of investigated cnidarians are disintegrated, indicating that microsynteny conservation is largely lost. In line with that, we find no evidence for topologically associated domains, suggesting fundamental difference in long-range gene regulation compared to vertebrates. However, both sea anemone genomes show remarkable chromosomal conservation with other cnidarians, several bilaterians and the sponge Ephydatia muelleri, allowing us to reconstruct the putative cnidarian and metazoan chromosomes, consisting of 19 and 16 ancestral linkage groups, respectively. These data suggest that large parts of the ancestral metazoan genome have been retained in chromosomes of some extant lineages, yet, higher order gene regulation may have evolved only after the cnidarian-bilaterian split.