Annelid functional genomics reveal the origins of bilaterian life cycles

Abstract

Indirect development with an intermediate larva exists in all major animal lineages1, which makes larvae central to most scenarios of animal evolution2–11. Yet how larvae evolved remains disputed. Here we show that temporal shifts (that is, heterochronies) in trunk formation underpin the diversification of larvae and bilaterian life cycles. We performed chromosome-scale genome sequencing in the annelid Owenia fusiformis with transcriptomic and epigenomic profiling during the life cycles of this and two other annelids. We found that trunk development is deferred to pre-metamorphic stages in the feeding larva of O. fusiformis but starts after gastrulation in the non-feeding larva with gradual metamorphosis of Capitella teleta and the direct developing embryo of Dimorphilus gyrociliatus. Accordingly, the embryos of O. fusiformis develop first into an enlarged anterior domain that forms larval tissues and the adult head12. Notably, this also occurs in the so-called ‘head larvae’ of other bilaterians13–17, with which the O. fusiformis larva shows extensive transcriptomic similarities. Together, our findings suggest that the temporal decoupling of head and trunk formation, as maximally observed in head larvae, facilitated larval evolution in Bilateria. This diverges from prevailing scenarios that propose either co-option9,10 or innovation11 of gene regulatory programmes to explain larva and adult origins.

Molecular evidence of anteroposterior patterning in adult echinoderms

“…These observations agree with previous reports that Hox expression in echinoderms is largely restricted to internal germ layers 25,26,29,30 and with the hox-driven O-A correlation observed in our RNA tomography dataset. In hemichordates and other bilaterians, Hox gene domains are intercalated during trunk development between the anterior domains and the posterior end of the animal, which expresses posteriorizing factors such as wnt3 39,43 . In P. miniata , we suggest that there is no ectoderm equivalent to a trunk region, because wnt3 is expressed at the edge of the ambulacral region, and because hox1 is the only Hox gene expressed in the ectoderm.…”

“…The mesoderm and endoderm trunk programs are surrounded by an ectoderm with two clear territories, including (1) an ambulacral anterior-like domain that is the main focus of our work, and also surprisingly (2) an extensive interambulacral domain that wraps around the aboral side of the animal and displays uncertain axial identity, without coherent deployment of the ancestral AP patterning program. The uncoupling of an ectodermal head and trunk programs is not unique to P. miniata and has been demonstrated in both larval echinoderms and hemichordates 39,47 , and recently in annelid larvae 43 , suggesting that these regulatory programs can be uncoupled over macroevolutionary time frames.…”

Insights into deuterostome evolution from the biphasic transcriptional programme of hemichordates

“…We compared all possible combinations of clusters of stage-specific genes between pairs of species by performing orthogroup overlap analysis (Martín-Zamora et al 2023; Marlétaz et al 2018). For a given cluster in species ‘a’ a.x and a given cluster in species ‘b’ b.y, we counted the number of overlapped orthogroups between a.x and b.y (the number of genes from a given orthogroup in clusters a.x and b.y), and subjected these to upper-tail hypergeometric test.…”

Evolution of homology: From archetype towards a holistic concept of cell type

“…Widespread, active enhancer demethylation only occurs later, during the phylotypic stage of development, when the vertebrate body plan and definitive organs are shaped, and is almost exclusively targeted towards genes with well-established critical roles in morphogenesis, including key developmental pathways, such as Wnt, Notch and transforming growth factor-β (Bogdanović et al, 2016). This wave of epigenetic remodelling coincides with the major transcriptomic and morphological transitions during the most conserved, phylotypic stage of ontogenesis (Drost et al, 2017;Levin et al, 2016;Martín-Zamora et al, 2023;Uesaka et al, 2022;L. Wu et al, 2019), thus suggesting the existence of an, at least, panvertebrate regulatory logic based on DNA methylation as a primal, upstream regulator of phylotypic enhancer activity.…”

“…Heterochronic module deployment is a salient and inherent feature of the cell developmental programme, whereby a variation in the tempo of state-state trajectories does not break its correct sequential execution. Thus, trunk patterning by HOX genes has been recently shown to have shifted from premetamorphic stages to early embryogenesis in the evolution of annelids, with such a heterochronic event being associated with noticeable changes in transcriptomic and chromatin remodelling in primitive vs. derived species (Martín-Zamora et al, 2023). This case study well illustrates the capacity of the developmental programme to 'condense,' in much the same manner as it had once occurred when all the life-cycle cell states once imprinted in the genome of a unicelled ancestor became executed by the first clonally multicellular holozoan.…”