An ancient genome duplication in the speciose reef-building coral genus, Acropora

Abstract

16Whole-genome duplication (WGD) has been recognized as a significant evolutionary 17 force in the origin and diversification of vertebrates, plants, and other organisms. 18Acropora, one of the most speciose reef-building coral genera, responsible for 19 creating spectacular but increasingly threatened marine ecosystems, is suspected to 20 have originated by polyploidy, yet there is no genetic evidence to support this 21 hypothesis. Using comprehensive phylogenomic and comparative genomic 22 approaches, we analyzed five Acropora genomes and an Astreopora genome 23 (Scleractinia: Acroporidae) to show that a WGD event likely occurred between 27.9 24 and 35.7 Million years ago (Mya) in the most recent common ancestor of Acropora, 25 concurrent with a massive worldwide coral extinction. We found that duplicated 26 genes became highly enriched in gene regulation functions, some of which are 27 involved in stress responses. The different functional clusters of duplicated genes are 28 related to the divergence of gene expression patterns during development. Some gene 29 duplications of proteinaceous toxins were generated by WGD in Acropora compared 30 with other Cnidarian species. Collectively, this study provides evidence for an ancient 31 WGD event in corals and it helps to explain the origin and diversification of Acropora. 32 gene families [12,13]. Thus, based on their unique lifestyle, variable chromosome 48 numbers, and complicated reticular evolutionary history, Indo-Pacific Acropora likely 49 originated via polyploidy [10][11][12][13][14][15][16]. However, there is no direct molecular and genetic 50 evidence to support this hypothesis. 51 52Ancient whole (large-scale)-genome duplication (WGD), or paleopolyploidy, has 53 shaped in the genomes of vertebrates, green plants, and other organisms, and is 54 usually regarded as an evolutionary landmark in the origins and diversification of 55 organisms [17][18][19] (Supplementary Fig. 1). Two separate WGD events have been 56 documented in the common ancestors of vertebrates (two-rounds of WGD) [20] and 57 4 another major WGD has been reported in the last common ancestor of teleost fish 58 [21,22]. Meanwhile, living angiosperms share an ancient WGD event [23,24], and 59 many other WGD events have been reported in major clades of angiosperms [25,26]. 60In addition, two-rounds of WGDs in the vertebrates are suggested to have occurred 61 during the Cambrian Period, and some WGDs in plants are believed to have occurred 62during Cretaceous-Tertiary [17,25,27]. Thus, WGD is regarded as an important 63 evolutionary way to reduce the risk of extinction [17,18,25]. However, the study of 64 WGD in Cnidaria has received less attention [17,18,[28][29][30]. 65 66 Duplicated genes created by WGD have complex fates following the time of 67 diploidization [18,31]. Usually, one of the duplicated genes is silenced or lost due to 68 redundancy of gene functions, termed "nonfunctionalization". However, retained 69 duplicated genes provide important sources of biological complexity and ev...