Journal
NATURE ECOLOGY & EVOLUTION
Volume 4, Issue 5, Pages -Publisher
NATURE PORTFOLIO
DOI: 10.1038/s41559-020-1138-1
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Funding
- National Natural Science Foundation of China [31871499, U1706203]
- National Key Research and Development Project [2018YFD0900206]
- Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) [2018SDKJ0302-1]
- major basic research projects of the Shandong Natural Science Foundation [ZR2018ZA0748]
- Fundamental Research Funds for the Central Universities [201762001, 201841001]
- China Postdoctoral Science Foundation [2018M642702]
- Taishan Scholar Project Fund of Shandong Province of China
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The transient larva-bearing biphasic life cycle is the hallmark of many metazoan phyla, but how metazoan larvae originated remains a major enigma in animal evolution. There are two hypotheses for larval origin. The 'larva-first' hypothesis suggests that the first metazoans were similar to extant larvae, with later evolution of the adult-added biphasic life cycle; the 'adult-first' hypothesis suggests that the first metazoans were adult forms, with the biphasic life cycle arising later via larval intercalation. Here, we investigate the evolutionary origin of primary larvae by conducting ontogenetic transcriptome profiling for Mollusca-the largest marine phylum characterized by a trochophore larval stage and highly variable adult forms. We reveal that trochophore larvae exhibit rapid transcriptome evolution with extraordinary incorporation of novel genes (potentially contributing to adult shell evolution), and that cell signalling/communication genes (for example, caveolin and innexin) are probably crucial for larval evolution. Transcriptome age analysis of eight metazoan species reveals the wide presence of young larval transcriptomes in both trochozoans and other major metazoan lineages, therefore arguing against the prevailing larva-first hypothesis. Our findings support an adult-first evolutionary scenario with a single metazoan larval intercalation, and suggest that the first appearance of proto-larva probably occurred after the divergence of direct-developing Ctenophora from a metazoan ancestor. Evolutionary analysis of transcriptomes across Metazoa supports a scenario of ancestral adult stages and a single intercalation event at the origin of larvae.
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