Skip to main content
SpringerLink
Log in

Adaptive Evolution Patterns in the Pacific Oyster Crassostrea gigas

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Estimation of adaptive evolution rates at the molecular level is important in evolutionary genomics. However, knowledge of adaptive evolutionary patterns in Mollusca is very scarce, especially for oysters. Such information would help clarify how oysters adapt to pathogen-rich and dynamically changing intertidal environments. In this study, we characterized the patterns of adaptive evolution in the Crassostrea gigas genome, using population diversity analysis and congeneric comparison. Our analysis revealed that gene expression patterns were positively associated with adaptive evolution rates, which suggested that positive selection played an important role in gene evolution. The genes with more exons and alternative splicing events had higher adaptive evolution rates. The rates of adaptive evolution in immune-related and stress-response genes were higher than those in other genes, suggesting that these groups of genes experienced strong positive selection. This study represents the first analysis of adaptive evolution rates in oysters and the first comprehensive study of a Mollusca species. These results provide a system-level investigation of association between adaptive evolution rates with some intrinsic genetic factors. They also suggest that adaptation to pathogens and environmental stressors are important forces driving the adaptive evolution of genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bachtrog D, Andolfatto P (2006) Selection, recombination and demographic history in Drosophila miranda. Genetics 174:2045–2059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, Hahn MW, Nista PM, Jones CD, Kern AD, Dewey CN, Pachter L, Myers E, Langley CH (2007) Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 5:2534–2559

    Article  CAS  Google Scholar 

  • Boyko AR, Williamson SH, Indap AR, Degenhardt JD, Hernandez RD, Lohmueller KE, Adams MD, Schmidt S, Sninsky JJ, Sunyaev SR (2008) Assessing the evolutionary impact of amino acid mutations in the human genome. PLoS Genet 4:e1000083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carneiro M, Albert FW, Melo-Ferreira J, Galtier N, Gayral P, Blanco-Aguiar JA, Villafuerte R, Nachman MW, Ferrand N (2012) Evidence for widespread positive and purifying selection across the European rabbit (Oryctolagus cuniculus) genome. Mol Biol Evol 29:1837–1849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Charlesworth J, Eyre-Walker A (2006) The rate of adaptive evolution in enteric bacteria. Mol Biol Evol 23:1348–1356

    Article  CAS  PubMed  Google Scholar 

  • Cutter AD, Payseur BA (2003) Selection at linked sites in the partial selfer Caenorhabditis elegans. Mol Biol Evol 20:665–673

    Article  CAS  PubMed  Google Scholar 

  • Derose-Wilson LJ, Gaut BS (2007) Transcription-related mutations and GC content drive variation in nucleotide substitution rates across the genomes of Arabidopsis thaliana and Arabidopsis lyrata. BMC Evol Biol 7:7

    Article  CAS  Google Scholar 

  • Eyre-Walker A, Keightley PD (2009) Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Mol Biol Evol 26:2097–2108

    Article  CAS  PubMed  Google Scholar 

  • Eyre-Walker A, Woolfit M, Phelps T (2006) The distribution of fitness effects of new deleterious amino acid mutations in humans. Genetics 173:891–900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fay JC, Wyckoff GJ, Wu CI (2001) Positive and negative selection on the human genome. Genetics 158:1227–1234

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galtier N (2016) Adaptive protein evolution in animals and the effective population size hypothesis. PLoS Genet 12:e1005774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gossmann TI, Song B-H, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A (2010) Genome wide analyses reveal little evidence for adaptive evolution in many plant species. Mol Biol Evol 27:1822–1832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guéguen L, Gaillard S, Boussau B, Gouy M, Groussin M, Rochette NC, Bigot T, Fournier D, Pouyet F, Cahais V (2013) Bio++: efficient extensible libraries and tools for computational molecular evolution. Mol Biol Evol 30:1745–1750

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Li C, Wang H, Xu Z (2018) Diversity and evolution of living oysters. J Shellfish Res 37:755–772

    Article  Google Scholar 

  • Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ram KR, Sirot LK, Levesque L, Artieri CG, Wolfner MF, Civetta A (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177:1321–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halligan DL, Keightley PD (2006) Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome research 16:875–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halligan DL, Oliver F, Eyre-Walker A, Harr B, Keightley PD (2010) Evidence for pervasive adaptive protein evolution in wild mice. PLoS Genet 6:e1000825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang B, Zhang L, Tang X, Zhang G, Li L (2016) Genome-wide analysis of alternative splicing provides insights into stress adaptation of the Pacific oyster. Mar Biotechnol 18:1–12

    Article  CAS  Google Scholar 

  • Hvilsom C, Qian Y, Bataillon T, Li Y, Mailund T, Sallé B, Carlsen F, Li R, Zheng H, Jiang T (2012) Extensive X-linked adaptive evolution in central chimpanzees. Proc Natl Acad Sci 109:2054–2059

    Article  PubMed  PubMed Central  Google Scholar 

  • Kousathanas A, Halligan DL, Keightley PD (2014) Faster-X adaptive protein evolution in house mice. Genetics 196:1131–1143

    Article  CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Proc GPD (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YL, Sun XQ, Hu XL, Xun XG, Zhang JB, Guo XM, Jiao WQ, Zhang LL, Liu WZ, Wang J, Li J, Sun Y, Miao Y, Zhang XK, Cheng TR, Xu GL, Fu XT, Wang YF, Yu XR, Huang XT, Lu W, Lv J, Mu C, Wang DW, Li X, Xia Y, Li YJ, Yang ZH, Wang FL, Zhang L, Xing Q, Dou HQ, Ning XH, Dou JZ, Li YP, Kong DX, Liu YR, Jiang Z, Li RQ, Wang S, Bao ZM (2017) Scallop genome reveals molecular adaptations to semi-sessile life and neurotoxins. Nat Commun 8:1721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C, Wang J, Song K, Meng J, Xu F, Li L, Zhang G (2018) Construction of a high-density genetic map and fine QTL mapping for growth and nutritional traits of Crassostrea gigas. BMC Genomics 19:626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V (2009) Population genomics of domestic and wild yeasts. Nature 458:337–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loire E, Chiari Y, Bernard A, Cahais V, Romiguier J, Nabholz B, Lourenço JM, Galtier N (2013) Population genomics of the endangered giant Galápagos tortoise. Genome Biol 14:R136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mcdonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654

    Article  CAS  PubMed  Google Scholar 

  • Nam B-H, Kwak W, Kim Y-O, Kim D-G, Kong HJ, Kim W-J, Kang J-H, Park JY, An CM, Moon J-Y (2017) Genome sequence of pacific abalone (Haliotis discus hannai): the first draft genome in family Haliotidae. Gigascience 6:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Obbard DJ, Welch JJ, Kim K-W, Jiggins FM (2009) Quantifying adaptive evolution in the Drosophila immune system. PLoS Genet 5:e1000698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel RK, Jain M (2012) NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277

    Article  CAS  PubMed  Google Scholar 

  • Sackton TB, Lazzaro BP, Schlenke TA, Evans JD, Dan H, Clark AG (2007) Dynamic evolution of the innate immune system in Drosophila. Nat Genet 39:1461–1468

    Article  CAS  PubMed  Google Scholar 

  • Schlenke TA, Begun DJ (2003) Natural selection drives Drosophila immune system evolution. Genetics 164:1471–1480

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simakov O, Marletaz F, Cho S-J, Edsinger-Gonzales E, Havlak P, Hellsten U, Kuo D-H, Larsson T, Lv J, Arendt D (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493:526–531

    Article  CAS  PubMed  Google Scholar 

  • Smith NG, Eyre-Walker A (2002) Adaptive protein evolution in Drosophila. Nature 415:1022–1024

    Article  CAS  PubMed  Google Scholar 

  • Song K, Li YX, Huang BY, Li L, Zhang GF (2017) Genetic and evolutionary patterns of innate immune genes in the Pacific oyster Crassostrea gigas. Dev Comp Immunol 77:17–22

    Article  CAS  PubMed  Google Scholar 

  • Song K, Li L, Zhang G (2018) Relationship among intron length, gene expression, and nucleotide diversity in the Pacific oyster Crassostrea gigas. Mar Biotechnol 20:676–684

  • Sun J, Zhang Y, Xu T, Zhang Y, Mu H, Zhang Y, Lan Y, Fields CJ, Hui JHL, Zhang W (2017) Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes. Nat Ecol Evol 1:0121

    Article  Google Scholar 

  • Tsagkogeorga G, Cahais V, Galtier N (2012) The population genomics of a fast evolver: high levels of diversity, functional constraint, and molecular adaptation in the tunicate Ciona intestinalis. Genome Biol Evol 4:852–861

    Article  CAS  PubMed Central  Google Scholar 

  • Veeramah KR, Gutenkunst RN, Woerner AE, Watkins JC, Hammer MF (2014) Evidence for increased levels of positive and negative selection on the X chromosome versus autosomes in humans. Mol Biol Evol 31:2267–2282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vincent R, Sébastien H, Frédéric D, Douzery EJP (2011) MACSE: multiple alignment of coding SEquences accounting for frameshifts and stop codons. PLoS One 6:e22594

    Article  CAS  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Zhang J, Jiao W, Li J, Xun X, Sun Y, Guo X, Huan P, Dong B, Zhang L (2017a) Scallop genome provides insights into evolution of bilaterian karyotype and development. Nat Ecol Evol 1:0120

    Article  Google Scholar 

  • Wang X, Wang M, Jia Z, Qiu L, Wang L, Zhang A, Song L (2017b) A carbonic anhydrase serves as an important acid-base regulator in pacific oyster Crassostrea gigas exposed to elevated CO 2: implication for physiological responses of mollusk to ocean acidification. Mar Biotechnol 19:22–35

    Article  CAS  Google Scholar 

  • Wei L, Xu F, Wang Y, Cai Z, Yu W, He C, Jiang Q, Xu X, Guo W, Wang X (2018) The molecular differentiation of anatomically paired left and right mantles of the Pacific oyster Crassostrea gigas. Mar Biotechnol 20:425–435

  • Xu B, Yang Z (2013) PAMLX: a graphical user interface for PAML. Mol Biol Evol 30:2723–2724

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Li Q, Yu H, Kong L (2017) Estimates of heritability for growth and shell color traits and their genetic correlations in the black shell strain of pacific oyster Crassostrea gigas. Mar Biotechnol 19:421–429

    Article  CAS  Google Scholar 

  • Yue C, Li Q, Yu H (2018) Gonad transcriptome analysis of the Pacific oyster Crassostrea gigas identifies potential genes regulating the sex determination and differentiation process. Mar Biotechnol 20:206–219

    Article  CAS  Google Scholar 

  • Zhang GF, Fang XD, Guo XM, Li L, Luo RB, Xu F, Yang PC, Zhang LL, Wang XT, Qi HG, Xiong ZQ, Que HY, Xie YL, Holland PWH, Paps J, Zhu YB, Wu FC, Chen YX, Wang JF, Peng CF, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang ZY, Zhu QH, Feng Y, Mount A, Hedgecock D, Xu Z, Liu YJ, Domazet-Loso T, Du YS, Sun XQ, Zhang SD, Liu BH, Cheng PZ, Jiang XT, Li J, Fan DD, Wang W, Fu WJ, Wang T, Wang B, Zhang JB, Peng ZY, Li YX, Li N, Wang JP, Chen MS, He Y, Tan FJ, Song XR, Zheng QM, Huang RL, Yang HL, Du XD, Chen L, Yang M, Gaffney PM, Wang S, Luo LH, She ZC, Ming Y, Huang W, Zhang S, Huang BY, Zhang Y, Qu T, Ni PX, Miao GY, Wang JY, Wang Q, Steinberg CEW, Wang HY, Li N, Qian LM, Zhang GJ, Li YR, Yang HM, Liu X, Wang J, Yin Y, Wang J (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54

    Article  CAS  PubMed  Google Scholar 

  • Zhang N, Xu F, Guo X (2014) Genomic analysis of the Pacific oyster (Crassostrea gigas) reveals possible conservation of vertebrate sex determination in a mollusc. G3 (Bethesda) 4:2207–2217

  • Zhang L, Li L, Guo X, Litman GW, Dishaw LJ, Zhang G (2015a) Massive expansion and functional divergence of innate immune genes in a protostome. Sci Rep 5:8693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Sun J, Mu HW, Li J, Zhang YH, Xu FJ, Xiang ZM, Qian PY, Qiu JW, Yu ZN (2015b) Proteomic basis of stress responses in the gills of the Pacific oyster Crassostrea gigas. J Proteome Res 14:304–317

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Yu H, Kong L, Liu S, Li Q (2015) Comparative transcriptome analysis of two oysters, Crassostrea gigas and Crassostrea hongkongensis provides insights into adaptation to hypo-osmotic conditions. Plos One 9:e111915

  • Zhao X, Yu H, Kong L, Li Q (2016) Gene co-expression network analysis reveals the correlation patterns among genes in euryhaline adaptation of Crassostrea gigas. Mar Biotechnol 18:535–544

    Article  CAS  Google Scholar 

Download references

Funding

This research was supported by the National Natural Science Foundation of China (11701546, 31530079).

Author information

Author notes

  1. Kai Song and Shiyong Wen contributed equally to this work.

Authors and Affiliations

  1. School of Mathematics and Statistics, Qingdao University, Qingdao, 266071, Shandong, China

    Kai Song

  2. College of Veterinary Medicine, Inner Mongolia Agricultural University, Huhhot, 010018, China

    Shiyong Wen

  3. Dezhou State-owned Assets Supervision and Administration Commission, Dezhou,, 253000, China

    Shiyong Wen

  4. Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, Shandong, China

    Guofan Zhang

Authors
  1. Kai Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shiyong Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guofan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kai Song or Guofan Zhang.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(DOCX 213 kb)

ESM 2

(XLSX 2748 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, K., Wen, S. & Zhang, G. Adaptive Evolution Patterns in the Pacific Oyster Crassostrea gigas. Mar Biotechnol 21, 614–622 (2019). https://doi.org/10.1007/s10126-019-09906-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-019-09906-w

Keywords

Search

Navigation