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.
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All sequencing data have been deposited at the NCBI’s SRA database under bioproject no. PRJNA562987.
The software and codes used in this study are publicly available, with corresponding versions indicated in Methods.
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We thank W. Liu and Y. Sun for help with SEM analysis of trochophore larvae and C. Cui for help with transcriptomic data analyses. We thank C. Zhao for providing zebrafish embryos and D. Chourrout for helpful discussions. We acknowledge support from the National Natural Science Foundation of China (grant no. U1706203), National Key Research and Development Project (grant no. 2018YFD0900206), National Natural Science Foundation of China (grant no. 31871499), Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (grant no. 2018SDKJ0302-1), major basic research projects of the Shandong Natural Science Foundation (grant no. ZR2018ZA0748), Fundamental Research Funds for the Central Universities (grant nos. 201762001 and 201841001), China Postdoctoral Science Foundation Funded Project (grant no. 2018M642702) and the Taishan Scholar Project Fund of Shandong Province of China.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
(a) Totally 19,189 genes are expressed (TPM>1) in at least one of 16 ontogenetic transcriptomes and 17.5% of them are universally expressed in all the samples. (b) Comparison of expressed genes among various stages of the whole life cycle.
(a) Distribution of gene expression levels for transcription factors (TFs) (orange) and all genes (blue) across different ontogenetic stages. In all samples, TF genes have higher average expression than all genes. The black lines inside the box indicate the median values, and the whiskers extend from the first or third quartiles to the minimum or maximum values. (b) Numbers of TFs expressed in each sample (blue bars) and the proportion of expressed TFs versus all expressed genes, given as a percentage (red points). The numbers of expressed TFs vary in different samples, ranging from 331 in the 2-8cell stage to 577 in the juvenile scallop. In all samples, TFs constitute ~4% of all expressed genes. (c) The expression of ubiquitous TFs spans almost six orders of magnitude while the expression of stage-restricted expressed TFs was usually high but restricted in certain ontogenetic stages. For each ontogenetic stage, gene names are shown for the top five TFs with the largest fold change relative to the average expression level of all other stages. The ubiquitous and restricted TFs are indicated in blue and red, respectively.
Histograms show the distribution of old genes (blue) and young (Bivalvia-specific or Gastropoda-specific) or novel (species-specific) genes (red) among top500 highly expressed genes for each molluscan species. There is a general tendency of higher representation of young/novel genes over old genes among 11 molluscan mantle transcriptomes. The statistical significance was evaluated using the Chi-Square test. **, p <0.05; *, p <0.01.
Extended Data Fig. 4 Distribution of young/novel genes in the group of mantle-exclusive expressed genes and the group of trochophore-mantle shared expressed genes.
Histograms show the distribution of young/novel genes in the group of mantle-exclusive expressed genes (blue) and the group of trochophore-mantle shared genes (red). There is significantly higher representation of novel or young genes in the group of trochophore-mantle shared genes over the group of mantle-exclusive expressed genes (one-sided paired t-test, p-value = 0.008).
Extended Data Fig. 5 Expression patterns of four highly expressed novel genes at scallop trochophore stage.
(a) Whole mount in situ hybridization of four novel genes (T21316, T16918, T04332, T22991). The spatial expression patterns of T21316 and T16918 showed full-range of the shell field while T04332 and T22991 showed marginal expression around the shell field, which suggested their involvement in the early formation of shell field at the trochophore stage. (b) Expression levels of these novel genes showed their high (TPM: 5,475-40,410) and restricted expression in trochophore but drastic decreased expression at fully shell-formed larval stages and barely no expression in adult mantle (TPM: 0.1-1.2).
Extended Data Fig. 6 Transcriptome age index (TAI) across the ontogeny of eight primary larva-bearing animals.
The TAI values of developmental stages are shown for all individual phylostratum levels. The “young-larval-transcriptome” feature is generally observed across Metazoa, supporting the evolutionarily latter appearance of primary larval stages. For H. discus hannai, although such feature is not evident at the last PS level (ps11), it is evident at older PS levels (e.g., ps4-ps10). E, L and AL represent embryonic, larva and adult-like stages.
Extended Data Fig. 7 Spatial expression of larva-related genes in the trochophore larvae of mollusc P. yessoensis and annelid U. unicinctus, in comparison to the direct-developing vertebrate D. rerio.
Whole mount in situ hybridization of caveolin, innexin and ATP1B genes (with the highest expression at the trochophore stage) in the mollusc P. yessoensis and the annelid U. unicinctus. In comparison, spatial expression patterns of two ATP1B genes (ATP1B1a, ATP1B2a) are shown for three ontogenetic stages (early/mid/late somitogenesis after gastrulation) of the direct-developing vertebrate D. rerio. The major expression sites of caveolin and innexin genes were at the apical organ and ciliary bands – the major larval features of trochophore. The expression of ATP1B largely corresponds to the forthcoming adult territory in both indirect-developing and direct-developing animals. No signal in the control group using sense probes confirmed the reliability of the positive signals. at, apical tuft; pt, prototroch; sfi, shell field invagination; tt, telotroch; cc, circumpharyngeal connective; vn, ventral nerve cord; 12 S, 12-somite stage; 18 S, 18-somite stage; 24 hpf, 24 hours post fertilization.
Extended Data Fig. 8 Ontogenetic expression profiling of trochozoan larva-related genes and their spatial expression in early developmental stages of scallop.
(a–d) Expression levels of caveolin, innexin and ATP1B genes in four trochozoans P. yessoensis, U. unicinctus, H. discus hannai and C. gigas. In comparison. ATP1B shows stronger early-expression over caveolin/innexin during early developmental stages. (e) Left panel: whole mount in situ hybridization of caveolin, innexin and ATP1B genes in early developmental stages of scallop. The major expression sites of caveolin and innexin genes were largely correspond to the regions with forthcoming larval characteristic features whereas the expression of ATP1B largely corresponds to the forthcoming adult territory (sfi /sf). No signal in the control group using sense probes confirmed the reliability of observed positive signals. Right panel: the scanning electron microscopy (SEM) micrograph of the trochophora larva of scallop P. yessoensis. sfi, shell field invagination; at, apical tuft; pt, prototroch; sf, shell field; cf, ciliated field.
Extended Data Fig. 9 Comparison of relative larval TAI contribution between ps4 and other phylostratum levels.
Across eight metazoan species, the larval TAI contribution by the genes of ps4 is significantly larger than those by other phylotratum levels (except ps11), implicating ps4 (Metazoa) as the potential timing of single proto-larva origin. For each phylotratum, the larval TAI contribution was normalized by fold difference relative to the average value across eight metazoan species. The lines inside the box indicate the median values, the whiskers extend from the first or third quartiles to the minimum or maximum values and the dots show individual data points. For comparisons of ps4 with other phylostratum levels, statistical significance based on one-sided t-test is shown on the top of each box.
Extended Data Fig. 10 Across-Metazoa TAI comparison of three developmental groups (embryonic, primary larva and adult-like/adult).
Based on the TAI data from eight metazoan species, box plots show significantly high TAIs contributed by either all genes (a) or the genes of ps4 (b) in the larval group over embryonic and adult-like/adult groups. For each species, TAI value was normalized by fold difference relative to the average value of TAIs(N) across the ontogeny. The lines inside the box indicate the median values, the whiskers extend from the first or third quartiles to the minimum or maximum values and the dots show individual data points. Statistical significance (p-value based on one-sided t-test) is shown above each box pair in comparison.
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Wang, J., Zhang, L., Lian, S. et al. Evolutionary transcriptomics of metazoan biphasic life cycle supports a single intercalation origin of metazoan larvae. Nat Ecol Evol 4, 725–736 (2020). https://doi.org/10.1038/s41559-020-1138-1
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