Single-cell atlases of two lophotrochozoan larvae highlight their complex evolutionary histories

Abstract

Pelagic larval stages are widespread across animals, yet it is unclear if larvae were present in the last common ancestor of animals or whether they evolved multiple times due to common selective pressures. Many marine larvae are at least superficially similar, they are small, swim through beating of ciliated bands and sense the environment with an apical organ structure. To understand these similarities, we have generated single cell atlases for marine larvae from two animal phyla and have compared their cell types. We found clear similarities among ciliary band cells and neurons of the apical organ in the two larvae pointing to possible homology of these structures suggesting a single origin of larvae within the clade analysed here (Lophotrochozoa). We also find several clade specific innovations in each larva, including distinct myocytes and shell gland cells in the oyster larva. Oyster shell gland cells express many novel genes which have made previous gene age estimates for trochophore larvae too young.

Duplication and Losses of Opsin Genes in Lophotrochozoan Evolution

“…Little is known about the Lophotrochocoan common ancestor (LOCA) that appeared in the Ediacaran. Based on the comparisons between the trochophore larvae (mollusc-like larvae) and the Muller larvae (polyclad-like larvae), it has recently been speculated that LOCA might have possessed a swimming larval stage ( Piovani et al 2023 ). The adult, in contrast, might have had a more benthic lifestyle resembling animals like Kimberella quadrata ( Fedonkin and Waggoner 1997 ).…”

An ancient gene regulatory network sets the position of the forebrain in chordates

“…AOs have long been at the centre of the debate on the evolution of nervous systems. The reason for their evolutionary relevance is that AOs are present in the ciliated primary larvae of a number of taxa across metazoans, including cnidarians, spiralian protostomes and ambulacrarian deuterostomes (Echinodermata + Hemichordata) 12,13,20,93 . AOs are therefore one of the few unifying features across distantly related animals with the most diverse neural architectures, ranging from nerve nets to ventrally centralized nerve cords 12,14,17,22,24,28,[94][95][96][97] .…”

“…The reason for their evolutionary relevance is that AOs are present in the ciliated primary larvae of a number of taxa across metazoans, including cnidarians, spiralian protostomes and ambulacrarian deuterostomes (Echinodermata + Hemichordata) 12,13,20,93 . AOs are therefore one of the few unifying features across distantly related animals with the most diverse neural architectures, ranging from nerve nets to ventrally centralized nerve cords 12,14,17,22,24,28,[94][95][96][97] . Given this, the absence of AOs in chordates has given rise to numerous hypotheses aiming to explain the loss of AOs and gain of a dorsally centralized neural tube in this group of animals.…”

“…The other two deuterostome phyla, echinoderms and hemichordates, lack an identifiable brain, and the derived pentaradial organization of the echinoderm body makes evolutionary comparisons challenging 4,5 . However, a common aspect of nervous system development in ambulacrarians (echinoderms and hemichordates), also shared with protostomes [6][7][8][9][10][11][12] and cnidarians [13][14][15] , is the presence of larval apical organs (AO) [16][17][18] . These are sensory-neurosecretory structures that develop from the anteriormost part of the ectoderm in all these phyla 19,20 , suggesting that the apical gene regulatory network (aGRN) specifying AOs might have appeared with the ancestor of Eumetazoa (Cnidaria + Bilateria (Protostomes + Deuterostomes)) [20][21][22] .…”

Single-Cell Automated Annotation Algorithm Based on Reference Expression Profiles

“…Through extensive iterative testing, the dataset was partitioned into reference and test datasets at a specific ratio, guided by known biological correlations [24] . This rigorous process was implemented to ensure that the gene sets employed faithfully reflect the distinctive features of each cell type [25,26] .…”