Skip to main content
SpringerLink
Log in

Life-history traits display strong associations to genome size in annelids

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Genome size, known also as the C-value, has been proposed as an important determinant of life-history variation in numerous animal taxa. We assessed the relationships between genome size and fitness-related life-history traits in six species of interstitial marine annelids of the genus Ophryotrocha. Life-history traits and genome size data obtained from 18 additional annelid species were included in our analyses to have a broader phylogenetic scope. Unexpectedly, genome sizes assessed here by flow cytometry in four Ophryotrocha species were three times larger than previously reported values obtained using Feulgen densitometry. This has implications for the hypothesis that harsh interstitial habitats select for small genomes in meiofaunal annelids. Within the genus Ophryotrocha, significant and positive relationships were found between genome size and nucleus size, and between genome size, age at first egg mass deposition, body size and lifespan. These relationships held up in the broader phylogenetic comparison. Our study provides evidence for the important role played by genome size in the evolution of life-history traits in annelids.

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.

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

Similar content being viewed by others

Data availability

We have deposited the primary data underlying these analyses as follows: Sampling locations, morphological data and microsatellite genotypes: Dryad DNA sequences: Genbank accessions Branchiura sowerbyi (LN810299.1, KY636792.1), Cerebratulus lacteus (KC698905.1, KX261740.1), Erpobdella obscura (AF003273.1, JQ821464.1), Hirudo medicinalis (EF446704.1, AF315058.1), Laeonereis culveri (MH235843, MH264663.1), Limnodrilus hoffmeisteri (LN810304.1, AY885613.1), Limnodrilus udekemianus (LN810320.1, KY636789.1), Lumbriculus variegatus (FJ639308.1, AY521550.1), Myxicola infundibulum (HQ024104.1, HM800977.1), Neanthes acuminata (KJ539071.1, KJ538996.1), Nephtys incisa (KT307667.1, GU179356.1), Ophidonais serpentina (LN810257.1, DQ459939.1), Ophryotrocha adherens (MK933737, MT737363.1), Ophryotrocha japonica (MK933739, MT737362.1), Ophryotrocha diadema (MK933738, MT737364.1), Ophryotrocha labronica (MK933740, MT737361.1), Ophryotrocha puerilis (MK933741, MT737365.1), Ophryotrocha robusta (MK933742, MT737360.1), Platynereis dumerilii (KP127954.1, KP640622.1), Polygordius appendiculatus (KF808170.1, MG603472.1), Scalibregma inflatum (GU672569.1, KF511816.1), Spirosperma ferox (KY636947.1, KY636799.1), Syllis prolifera (JF903780.1, JF903739.1), Tubifex tubifex (HM138034.1, AF326005.1).

Data citation

The main dataset has been assembled and presented here as supplementary material.

References

  • Adreani, L., C. Bonacina, G. Bonomi, & C. Monti, 1984. Cohort cultures of Psammoryctides barbatus (Grube) and Spirosperma ferox Eisen: a tool for a better understanding of demographic strategies in Tubificidae. Hydrobiologia 115: 113–119.

    Article  Google Scholar 

  • Alfsnes, K., H. P. Leinaas, & D. O. Hessen, 2017. Genome size in arthropods; different roles of phylogeny, habitat and life history in insects and crustaceans. Ecology and evolution 7: 5939–5947.

    Article  PubMed  PubMed Central  Google Scholar 

  • Belzile, C., & M. Gosselin, 2015. Free-living stage of the unicellular algae Coccomyxa sp. parasite of the blue mussel (Mytilus edulis): Low-light adaptation, capacity for growth at a very wide salinity range and tolerance to low pH. Journal of Invertebrate Pathology 132: 201–207.

    Article  CAS  PubMed  Google Scholar 

  • Block, E. M., G. Moreno, & C. J. Goodnight, 1981. Observations on the life history of Limnodrilus hoffmeisteri (Annelida, Tubificidae) from the Little Calumet River in temperate North America. International Journal of Invertebrate Reproduction 4: 239–247.

    Article  Google Scholar 

  • Bonacina, C., A. Pasteris, G. Bonomi, & D. Marzuoli, 1994. Quantitative observations on the population ecology of Branchiura sowerbyi (Oligochaeta, Tubificidae). Hydrobiologia 278: 267–274.

    Article  Google Scholar 

  • Cavalier–Smith, T. (ed), 1985. The Evolution of Genome Size. Wiley-Blackwell, Chichester.

    Google Scholar 

  • Chakravarti, L. J., M. D. Jarrold, E. M. Gibbin, F. Christen, G. Massamba‐N’Siala, P. U. Blier, & P. Calosi, 2016. Can trans-generational experiments be used to enhance species resilience to ocean warming and acidification?. Evolutionary Applications 9: 1133–1146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dean, D., S. R. Chapman, & C. S. Chapman, 1987. Reproduction and development of the sabellid polychaete Myxicola infundibulum. Journal of the Marine Biological Association of the United Kingdom 67: 431–439.

    Article  Google Scholar 

  • Ducrot, V., A. R. R. Péry, H. Quéau, R. Mons, M. Lafont, & J. Garric, 2007. Rearing and estimation of life-cycle parameters of the tubicifid worm Branchiura sowerbyi: application to ecotoxicity testing. The Science of the Total Environment 384: 252–263.

    Article  CAS  PubMed  Google Scholar 

  • Dufresne, F., & N. Jeffery, 2011. A guided tour of large genome size in animals: what we know and where we are heading. Chromosome Research 19: 925–938.

    Article  CAS  PubMed  Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5): 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández, J., & G. S. Stent, 1982. Embryonic development of the hirudinid leech Hirudo medicinalis: structure, development and segmentation of the germinal plate. Journal of Embryology and Experimental Morphology 72: 71–96.

    PubMed  Google Scholar 

  • Fischer, A., & A. Dorresteijn, 2004. The polychaete Platynereis dumerilii (Annelida): a laboratory animal with spiralian cleavage, lifelong segment proliferation and a mixed benthic/pelagic life cycle. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 26: 314–325.

    Google Scholar 

  • Fraipont, J., 1887. Le genre Polygordius. Engelmann.

  • Galbraith, D. W., K. R. Harkins, J. M. Maddox, N. M. Ayres, D. P. Sharma, & E. Firoozabady, 1983. Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220: 1049–1051.

    Article  CAS  PubMed  Google Scholar 

  • Gambi, M. C., L. Ramella, G. Sella, P. Protto, & E. Aldieri, 1997. Variation in Genome Size in Benthic Polychaetes: Systematic and Ecological Relationships. Journal of the Marine Biological Association of the United Kingdom 77: 1045–1057.

    Article  Google Scholar 

  • Gibbin, E. M., L. J. Chakravarti, M. D. Jarrold, F. Christen, V. Turpin, G. M. N’Siala, P. U. Blier, & P. Calosi, 2017a. Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life history and physiology in a marine metazoan?. Journal of Experimental Biology 220: 551–563.

    PubMed  Google Scholar 

  • Gibbin, E. M., G. Massamba N’Siala, L. J. Chakravarti, M. D. Jarrold, & P. Calosi, 2017b. The evolution of phenotypic plasticity under global change. Scientific Reports 7: 1–8.

    Article  CAS  Google Scholar 

  • Grandi, V., 2009. Nicchia ecologica, storie vitali e morfologia. PhD Thesis, XXII cycle, Università di Modena e Reggio Emilia.

  • Gregory, T. R., 2002. Genome size and developmental parameters in the homeothermic vertebrates. Genome 45: 833–838.

    Article  CAS  PubMed  Google Scholar 

  • Gregory, T. R., 2005. The C-value enigma in plants and animals: a review of parallels and an appeal for partnership. Annals of Botany 95: 133–146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory, T. R., 2020. Animal Genome Size Database. Animal Genome Size Database, http://www.genomesize.com.

  • Griffith, O. L., G. E. E. Moodie, & A. Civetta, 2003. Genome size and longevity in fish. Experimental Gerontology 38: 333–337.

    Article  CAS  PubMed  Google Scholar 

  • Hardie, D. C., & P. D. Hebert, 2011. Genome-size evolution in fishes. Canadian Journal of Fisheries and Aquatic Sciences 61:1636-1646

    Article  Google Scholar 

  • Hardie, D. C., T. R. Gregory, & P. D. N. Hebert, 2002. From pixels to picograms: a beginners’ guide to genome quantification by Feulgen image analysis densitometry. The Journal of Histochemistry and Cytochemistry 50: 735–749.

    Article  CAS  PubMed  Google Scholar 

  • Hessen, D. O., & J. Persson, 2009. Genome size as a determinant of growth and life-history traits in crustaceans. Biological Journal of the Linnean Society 98: 393–399.

    Article  Google Scholar 

  • Hickey, A. J. R., & K. D. Clements, 2005. Genome Size Evolution in New Zealand Triplefin Fishes. Journal of Heredity 96: 356–362.

    Article  CAS  PubMed  Google Scholar 

  • Jalal, M., M. W. Wojewodzic, C. M. M. Laane, & D. O. Hessen, 2013. Larger Daphnia at lower temperature: a role for cell size and genome configuration?. Genome 56: 511–519.

    Article  CAS  PubMed  Google Scholar 

  • Jarrold, M. D., L. J. Chakravarti, E. M. Gibbin, F. Christen, G. Massamba-N’Siala, P. U. Blier, & P. Calosi, 2019. Life-history trade-offs and limitations associated with phenotypic adaptation under future ocean warming and elevated salinity. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 20180428.

    Article  Google Scholar 

  • Jeffery, N. W., E. A. Ellis, T. H. Oakley, & T. R. Gregory, 2017. The Genome Sizes of Ostracod Crustaceans Correlate with Body Size and Evolutionary History, but not Environment. The Journal of Heredity 108: 701–706.

    Article  PubMed  Google Scholar 

  • Jockusch, E. L., 1997. An evolutionary correlate of genome size change in plethodontid salamanders. Proceedings of the Royal Society B: Biological Sciences 264: 597.

    Article  CAS  PubMed Central  Google Scholar 

  • Kennedy, C. R., 1966. The Life History of Limnodrilus Udekemianus Clap. (Oligochaeta: Tubificidae). Oikos 17: 10–18.

    Article  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., & F. U. Battistuzzi, 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547–1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lefébure, T., C. Morvan, F. Malard, C. François, L. Konecny-Dupré, L. Guéguen, M. Weiss-Gayet, A. Seguin-Orlando, L. Ermini, C. D. Sarkissian, N. P. Charrier, D. Eme, F. Mermillod-Blondin, L. Duret, C. Vieira, L. Orlando, & C. J. Douady, 2017. Less effective selection leads to larger genomes. Genome Research 27: 1016–1028.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leiva, F. P., P. Calosi, & W. C. E. P. Verberk, 2019. Scaling of thermal tolerance with body mass and genome size in ectotherms: a comparison between water- and air-breathers. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 20190035.

    Article  Google Scholar 

  • Linton, D. L., & G. L. Taghon, 2000. Feeding, growth, and fecundity of Capitella sp. I in relation to sediment organic concentration. Marine Ecology Progress Series 205: 229–240.

    Article  Google Scholar 

  • Lynch, M., & J. S. Conery, 2003. The origins of genome complexity. Science 302: 1401–1404.

    Article  CAS  PubMed  Google Scholar 

  • Mackie, A. S. Y., 1991. Scalibregma Celticum New Species (Polychaeta: Scalibregmatidae) from Europe, with a Redescription of Scalibregma Inflatum Rathke, 1843 and Comments on the Genus Sclerobregma Hartman, 1965. Bulletin of Marine Science University of Miami - Rosenstiel School of Marine and Atmospheric Science 48: 268–276.

  • Martin, J., & R. Bastida, 2006a. Population structure, growth and production of Laeonereis culveri (Nereididae: Polychaeta) in tidal £ats of R|¤ o de la Plata estuary, Argentina. Journal of the Marine Biological Association of the UK 86: 235–244.

    Article  Google Scholar 

  • Martin, J. P., & R. Bastida, 2006b. Life history and production of Capitella capitata (Polychaeta: Capitellidae) in Río de la Plata Estuary (Argentina). Thalassas 22: 25–38.

    Google Scholar 

  • Matisoff, G., X. Wang, & P. L. McCall, 1999. Biological Redistribution of Lake Sediments by Tubificid Oligochaetes: Branchiura sowerbyi and Limnodrilus hoffmeisteri/Tubifex tubifex. Journal of Great Lakes Research 25: 205–219.

    Article  Google Scholar 

  • Mazurkiewicz, M., 1975. Larval development and habits of Laeonereis culveri (Webster) (Polychaeta: Nereidae). The Biological Bulletin 149: 186–204.

    Article  PubMed  Google Scholar 

  • Miller, W. E., 2014. Phenotypic correlates of genome size in lepidoptera. The Journal of the Lepidopterists’ Society 68: 203–210.

    Article  Google Scholar 

  • Monaghan, P., & N. B. Metcalfe, 2000. Genome size and longevity. Trends in Genetics 16: 331–332.

    Article  CAS  PubMed  Google Scholar 

  • Nascimento, H. L. S., & R. G. Alves, 2009. The effect of temperature on the reproduction of Limnodrilus hoffmeisteri (Oligochaeta: Tubificidae). Zoologia (Curitiba) 26: 191–193.

    Article  Google Scholar 

  • Ohtaka, A., & T. Iwakuma, 1993. Redescription of Ophidonais serpentina (Müller, 1773) (Naididae, Oligochaeta) from Lake Yunoko, Central Japan, with record of the olgochaete composition in the lake. Japanese Journal of Limnology (Rikusuigaku Zasshi) 54: 251–259.

    Article  Google Scholar 

  • Olmo, E., 2003. Reptiles: a group of transition in the evolution of genome size and of the nucleotypic effect. Cytogenetic and Genome Research 101: 166–171.

    Article  CAS  PubMed  Google Scholar 

  • Paxton, H., & B. Åkesson, 2010. The Ophryotrocha labronica group (Annelida: Dorvilleidae) – with the description of seven new species. Zootaxa 2713: 1–24.

    Article  Google Scholar 

  • Prevedelli, D., G. M. N’siala & R. Simonini, 2006. Gonochorism vs. hermaphroditism: relationship between life history and fitness in three species of Ophryotrocha (Polychaeta: Dorvilleidae) with different forms of sexuality. Journal of Animal Ecology 75: 203–212.

  • Reish, D. J., 1957. The life history of the polychaetous annelid Neanthes caudata (Delle Chiaje), including a summary of development in the family Nereidae. Pacific Science 216–288.

    Google Scholar 

  • Ritchie, H., A. J. Jamieson, & S. B. Piertney, 2017. Genome size variation in deep-sea amphipods. Royal Society Open Science 4: 170862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sella, G., Redi, C. A., Ramella, L., Soldi, R., & M. C. Premoli, 1993. Genome size and karyotype length in some interstitial polychaete species of the genus (Dorvilleidae). Genome 36(4): 652–657.

    Article  CAS  PubMed  Google Scholar 

  • Simonini, R., & D. Prevedelli, 2003. Life history and demography of three populations of Ophryotrocha japonica (Polychaeta: Dorvilleidae). Marine Ecology Progress Series 258: 171–180.

    Article  Google Scholar 

  • Soldi, R., Ramella, L., Gambi, M.C., Sordino, P., & G. Sella, 1994. Genome size in polychaetes: relationship with body length and life habit. Memoires du Museum National d'Histoire Naturelle 162: 129–135.

  • Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stelzer, C.-P., S. Riss, & P. Stadler, 2011. Genome size evolution at the speciation level: the cryptic species complex Brachionus plicatilis(Rotifera). BMC Evolutionary Biology 11: 90.

    Article  PubMed  PubMed Central  Google Scholar 

  • Struck, T. H., C. Paul, N. Hill, S. Hartmann, C. Hösel, M. Kube, B. Lieb, A. Meyer, R. Tiedemann, G. Purschke, & C. Bleidorn, 2011. Phylogenomic analyses unravel annelid evolution. Nature 471: 95–98.

    Article  CAS  PubMed  Google Scholar 

  • Thornhill, D. J., T. G. Dahlgren, & K. M. Halanych. 2009. Chapter 13: The evolution and ecology of Ophryotrocha(Dorvilleidae, Eunicida). pp. 242–256 in D. H. Shain, ed. Annelids as model systems in the biological sciences. JohnWiley & Son, Hoboken, NJ. (18) (PDF) Evolution and Ecology of Ophryotrocha (Dorvilleidae, Eunicida). Available from: https://www.researchgate.net/publication/230009592_Evolution_and_Ecology_of_Ophryotrocha_Dorvilleidae_Eunicida. Accessed 2 Dec 2020.

  • Timm, T., 2020. Observations on the life cycles of aquatic Oligochaeta in aquaria. Zoosymposia 17: 102–120.

    Article  Google Scholar 

  • Tsutsumi, H., & T. Kikuchi, 1984. Study of the life history of Capitella capitata (Polychaeta: Capitellidae) in Amakusa, South Japan including a comparison with other geographical regions. Marine Biology 80: 315–321.

    Article  Google Scholar 

  • Vergilino, R., C. Belzile, & F. Dufresne, 2009. Genome size evolution and polyploidy in the Daphnia pulex complex (Cladocera: Daphniidae). Biological Journal of the Linnean Society 97: 68–79.

    Article  Google Scholar 

  • Wyngaard, G. A., E. M. Rasch, N. M. Manning, K. Gasser, & R. Domangue, 2005. The relationship between genome size, development rate, and body size in copepods. Hydrobiologia 532: 123–137.

    Article  CAS  Google Scholar 

  • Yu, J. P., W. Liu, C. L. Mai, & W. B. Liao, 2020. Genome size variation is associated with life-history traits in birds. Journal of Zoology 310: 255–260.

    Article  Google Scholar 

  • Zajac, R. N., & R. B. Whitlatch, 1988. Population ecology of the polychaete Nephtys incisa in Long Island sound and the effects of disturbance. Estuaries 11: 117–133.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr Valentina Grandi, Dr. Maria Pia Martino, Prof. Daniela Prevedelli, and Prof. Roberto Simonini and of the University of Modena and Reggio Emilia (Italy) for giving us access to the PhD thesis containing the life-history data of the Ophryotrocha species. The authors would like to thank Marie-Hélène Carignan for her help with the preparation of samples, Francis Beaudet for his help with the annelid cultures Astrid Tempestini for sharing DNA sequences to build our phylogenies and Madeleine-Zoé Corbeil-Robitaille for drawing the annelid silhouettes. We also thank the Natural Sciences and Engineering Research Council of Canada (NSERC : RGPIN-2015-06500 and RGPIN- 06349), the Programme Établissement de Nouveaux Chercheurs Universitaires of the Fonds de Recherche du Québec—Nature et Technologies (FRQNT: No. 199173), BORÉAS UQAR, and the European Union through the Marie Skłodowska-Curie Post-doctoral Fellowship (Proposal Number: 659359) for funding different members of this team (see Funding section).

Funding

This work was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) grant (RGPIN- 2020–05627), Programme Établissement de Nouveaux Chercheurs Universitaires of the Fonds de Recherche du Québec—Nature et Technologies (FRQNT, No.199173) awarded to PC, an NSERC grant (RGPIN- 06349) awarded to FD, a BORÉAS UQAR Grant awarded to PC, FD and GMN, and by the European Union through the Marie Skłodowska-Curie Post-doctoral Fellowship (EVOLMARIN project—Proposal Number: 659359) awarded to GMN.

Author information

Author notes

  1. Piero Calosi and France Dufresne have contributed equally to this work.

Authors and Affiliations

  1. Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski, QC, Canada

    Nicholas Beaudreau, Gloria Massamba-N’Siala, Claude Belzile, Piero Calosi & France Dufresne

  2. Centre d’Écologie Fonctionnelle et Évolutive (CEFE- CNRS), UMR 5175, Montpellier Cedex 5, France

    Gloria Massamba-N’Siala

Authors
  1. Nicholas Beaudreau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gloria Massamba-N’Siala
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claude Belzile
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Piero Calosi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. France Dufresne
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The experimental design and work have been conceived and planned by NB, GMN, PC and FD. Life-history data were extracted from the literature by NB and GMN. NB conducted genome size measurements under the supervision of CB and FD. NB conducted statistical analyses and results interpretation supervised by GMC, PC and FD. NB wrote the first draft of this manuscript supported by PC and FD. All authors contributed to the final version of this manuscript.

Corresponding author

Correspondence to France Dufresne.

Ethics declarations

Conflict of interest

We have no competing interests.

Ethical approval

All applicable international, national and/or institutional ethics guidelines for sampling, care and experimental use of organisms have been followed in this study.

Additional information

Handling editor: Diego Fontaneto.

Publisher's Note

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beaudreau, N., Massamba-N’Siala, G., Belzile, C. et al. Life-history traits display strong associations to genome size in annelids. Hydrobiologia 848, 799–810 (2021). https://doi.org/10.1007/s10750-020-04477-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-020-04477-7

Keywords

Search

Navigation