Marine Biology

, 163:215 | Cite as

Genotype-by-environment interactions during early development of the sea urchin Evechinus chloroticus

  • Natalí J. Delorme
  • Mary A. Sewell
Original paper


The increase in seawater temperature due to anthropogenic climate change is likely to affect population persistence and changes in distributional ranges of marine species. Adaptation to warmer environmental conditions will be determined by the presence of tolerant genotypes within a population. The present study determined the genotype-by-environment (G × E) interactions during early development of the New Zealand sea urchin Evechinus chloroticus cultured at 18 °C (mean annual temperature), 21 °C (ambient summer temperature) and 24 °C (+3 °C above ambient summer temperature). The experiment was performed in 3 experimental blocks using gametes from 3 males and 3 females crossed in all combinations (North Carolina II cross-breeding design), resulting in 9 families per experimental block (i.e., total of 27 families). Differences between female and male identities were quantified during cleavage and gastrulation: Reaction norms (i.e., interaction plots) showed a clear G × E interaction, with some genotypes performing better than others at high temperatures. Heritability during gastrulation was 0.51, indicating that 51 % of the variability corresponds to genetic variation. Overall, the present study shows that seawater temperature has a negative effect on early development of E. chloroticus; however, there are resilient genotypes in the studied population that could provide the genetic potential to adapt to future ocean conditions.


Seawater Temperature Additive Genetic Variance Total Phenotypic Variance Female Identity Abnormal Embryo 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors would like to thank Errol Murray and Peter Browne for helping with setup of the experiment; Brady Doak for providing necessary equipment for animal collection; Leonardo Zamora for helping with animal collection, spawning induction and sampling; and Erica Zarate for statistical assistance. NJD was supported by a Chilean Government Scholarship (Becas Chile, CONICYT).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of the animals were followed.


  1. Barker M (2013) Evechinus chloroticus. In: John ML (ed) Developments in aquaculture and fisheries science. Elsevier, Amsterdam, pp 355–368Google Scholar
  2. Bell G, Collins S (2008) Adaptation, extinction and global change. Evol Appl 1:3–16. doi: 10.1111/j.1752-4571.2007.00011.x CrossRefGoogle Scholar
  3. Butts IAE, Litvak MK (2007) Stock and parental effects on embryonic and early larval development of winter flounder Pseudopleuronectes americanus (Walbaum). J Fish Biol 70:1070–1087. doi: 10.1111/j.1095-8649.2007.01369.x CrossRefGoogle Scholar
  4. Byrne M, Przeslawski R (2013) Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories. Integr Comp Biol 53:582–596. doi: 10.1093/icb/ict049 CrossRefGoogle Scholar
  5. Calosi P, Rastrick SPS, Lombardi C, de Guzman HJ, Davidson L, Jahnke M, Giangrande A, Hardege JD, Schulze A, Spicer JI, Gambi M-C (2013) Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system. Phil Trans R Soc B. doi: 10.1098/rstb.2012.0444 Google Scholar
  6. Chang Y, Zhang W, Zhao C, Song J (2012) Estimates of heritabilities and genetic correlations for growth and gonad traits in the sea urchin Strongylocentrotus intermedius. Aquac Res 43:271–280. doi: 10.1111/j.1365-2109.2011.02825.x CrossRefGoogle Scholar
  7. Crean AJ, Marshall DJ (2008) Gamete plasticity in a broadcast spawning marine invertebrate. PNAS 105:13508–13513. doi: 10.1073/pnas.0806590105 CrossRefGoogle Scholar
  8. Crean AJ, Dwyer JM, Marshall DJ (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology 94:2575–2582. doi: 10.1890/13-0184.1 CrossRefGoogle Scholar
  9. Császár NBM, Ralph PJ, Frankham R, Berkelmans R, van Oppen MJH (2010) Estimating the potential for adaptation of corals to climate warming. PLoS One 5(3):e9751. doi: 10.1371/journal.pone.0009751 CrossRefGoogle Scholar
  10. Delorme NJ, Sewell MA (2013) Temperature limits to early development of the New Zealand sea urchin Evechinus chloroticus (Valenciennes 1846). J Therm Biol 38:218–224. doi: 10.1016/j.jtherbio.2013.02.007 CrossRefGoogle Scholar
  11. Delorme NJ, Sewell MA (2014) Temperature and salinity: two climate change stressors affecting early development of the New Zealand sea urchin Evechinus chloroticus. Mar Biol. doi: 10.1007/s00227-014-2480-0 Google Scholar
  12. Delorme NJ, Sewell MA (2016) Effects of warm acclimation on physiology and gonad development in the sea urchin Evechinus chloroticus. Comp Biochem Physiol A Mol Integr Physiol 198:33–40. doi: 10.1016/j.cbpa.2016.03.020 CrossRefGoogle Scholar
  13. Dix T (1970a) Biology of Evechinus chloroticus (Echinoidea: Echinometridae) from different localities: 1 general. N Z J Mar Fresh 4:91–116. doi: 10.1080/00288330.1970.9515331 CrossRefGoogle Scholar
  14. Dix T (1970b) Biology of Evechinus chloroticus (Echinoidea: Echinometridae) from different localities: 3 reproduction. N Z J Mar Fresh 4:385–405. doi: 10.1080/00288330.1970.9515355 CrossRefGoogle Scholar
  15. Eisen E, Saxton A (1983) Genotype by environment interactions and genetic correlations involving two environmental factors. Theor Appl Genet 67:75–86. doi: 10.1007/bf00303929 CrossRefGoogle Scholar
  16. Evans JP, Marshall DJ (2005) Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59:106–112. doi: 10.1111/j.0014-3820.2005.tb00898.x CrossRefGoogle Scholar
  17. Evans JP, García-gonzález F, Marshall DJ (2007) Sources of genetic and phenotypic variance in fertilization rates and larval traits in a sea urchin. Evolution 61:2832–2838. doi: 10.1111/j.1558-5646.2007.00227.x CrossRefGoogle Scholar
  18. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, EssexGoogle Scholar
  19. Fenwick G, Horning D (1980) Echinodermata of the Snares Islands, southern New Zealand. N Z J Mar Fresh 14:437–445. doi: 10.1080/00288330.1980.9515888 CrossRefGoogle Scholar
  20. Foo S, Byrne M (2016) Acclimatization and adaptive capacity of marine species in a changing ocean. Adv Mar Biol. doi: 10.1016/bs.amb.2016.06.001 Google Scholar
  21. Foo SA, Dworjanyn SA, Poore AGB, Byrne M (2012) Adaptive capacity of the habitat modifying sea urchin Centrostephanus rodgersii to ocean warming and ocean acidification: performance of early embryos. PLoS One 7(8):e42497. doi: 10.1371/journal.pone.0042497 CrossRefGoogle Scholar
  22. Foo SA, Dworjanyn SA, Khatkar MS, Poore AGB, Byrne M (2014) Increased temperature, but not acidification, enhances fertilization and development in a tropical urchin: potential for adaptation to a tropicalized eastern Australia. Evol Appl 7:1226–1237. doi: 10.1111/eva.12218 CrossRefGoogle Scholar
  23. Foo SA, Sparks KM, Uthicke S, Karelitz S, Barker M, Byrne M, Lamare M (2016) Contributions of genetic and environmental variance in early development of the Antarctic sea urchin Sterechinus neumayeri in response to increased ocean temperature and acidification. Mar Biol 163:1–11. doi: 10.1007/s00227-016-2903-1 CrossRefGoogle Scholar
  24. Franke ES (2005) Aspects of fertilization ecology in Evechinus chloroticus and Coscinasterias muricata. PhD-Biological Sciences, University of AucklandGoogle Scholar
  25. Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46:185–208. doi: 10.1146/annurev-genet-110711-155511 CrossRefGoogle Scholar
  26. Garner DM (1969) The seasonal range of sea temperature on the New Zealand shelf. N Z J Mar Fresh 3:201–208. doi: 10.1080/00288330.1969.9515289 CrossRefGoogle Scholar
  27. Green BS (2008) Maternal effects in fish populations. Adv Mar Biol 54:1–105. doi: 10.1016/S0065-2881(08)00001-1 CrossRefGoogle Scholar
  28. Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. PNAS 104:1745–1750. doi: 10.1073/pnas.0610108104 CrossRefGoogle Scholar
  29. Heath DD, Fox CW, Heath JW (1999) Maternal effects on offspring size: variation through early development of chinook salmon. Evolution 53:1605–1611. doi: 10.2307/2640906 CrossRefGoogle Scholar
  30. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New YorkGoogle Scholar
  31. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479. doi: 10.1038/nature09670 CrossRefGoogle Scholar
  32. Hutchings JA, Bishop TD, McGregor-Shaw CR (1999) Spawning behaviour of Atlantic cod, Gadus morhua: evidence of mate competition and mate choice in a broadcast spawner. Can J Fish Aquat Sci 56:97–104. doi: 10.1139/f98-216 CrossRefGoogle Scholar
  33. IPCC (2014) Climate change 2014: impact, adaptation and vulnerability. Working Group II Contribution to the IPCC 5th Assessment Report. Cambridge University Press, CambridgeGoogle Scholar
  34. Kelly MW, Padilla-Gamiño JL, Hofmann GE (2013) Natural variation and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus. Glob Change Biol 19:2536–2546. doi: 10.1111/gcb.12251 CrossRefGoogle Scholar
  35. Kvingedal R, Evans BS, Lind CE, Taylor JJU, Dupont-Nivet M, Jerry DR (2010) Population and family growth response to different rearing location, heritability estimates and genotype × environment interaction in the silver-lip pearl oyster (Pinctada maxima). Aquaculture 304:1–6. doi: 10.1016/j.aquaculture.2010.02.035 CrossRefGoogle Scholar
  36. Liu X, Xiang J, Chang Y, Ding J, Cao X (2004) Study on heritability of growth in the juvenile sea urchin Strongylocentrotus nudus. J Shellfish Res 23(2):593–597Google Scholar
  37. Liu X, Chang Y, Xiang J, Cao X (2005) Estimates of genetic parameters for growth traits of the sea urchin, Strongylocentrotus intermedius. Aquaculture 243:27–32. doi: 10.1016/j.aquaculture.2004.10.014 CrossRefGoogle Scholar
  38. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, SunderlandGoogle Scholar
  39. Meyer E, Davies S, Wang S, Willis BL, Abrego D, Juenger TE, Matz MV (2009) Genetic variation in responses to a settlement cue and elevated temperature in the reef-building coral Acropora millepora. Mar Ecol Prog Ser 392:81–92. doi: 10.3354/meps08208 CrossRefGoogle Scholar
  40. Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ (2013) Predicting evolutionary responses to climate change in the sea. Ecol Lett 16(12):1488–1500. doi: 10.1111/ele.12185 CrossRefGoogle Scholar
  41. Nagel MM, Sewell MA, Lavery SD (2015) Differences in population connectivity of a benthic marine invertebrate Evechinus chloroticus (Echinodermata: Echinoidea) across large and small spatial scales. Conserv Genet 16:965–978. doi: 10.1007/s10592-015-0716-2 CrossRefGoogle Scholar
  42. Nduwumuremyi A, Tongoona P, Habimana S (2013) Mating designs: helpful tool for quantitative plant breeding analysis. J Plant Breed Genet 1:117–129Google Scholar
  43. Pistevos JCA, Calosi P, Widdicombe S, Bishop JDD (2011) Will variation among genetic individuals influence species responses to global climate change? Oikos 120:675–689. doi: 10.1111/j.1600-0706.2010.19470.x CrossRefGoogle Scholar
  44. Salinas S, Brown Simon C, Mangel M, Munch Stephan B (2013) Non-genetic inheritance and changing environments. Non-Genet Inherit 1:38–50. doi: 10.2478/ngi-2013-0005 Google Scholar
  45. Schiel DR (2013) The other 93 %: trophic cascades, stressors and managing coastlines in non-marine protected areas. N Z J Mar Fresh 47:374–391. doi: 10.1080/00288330.2013.810161 CrossRefGoogle Scholar
  46. Schiel D, Kingsford MJ, Choat JH (1986) Depth distribution and abundance of benthic organisms and fishes at the subtropical Kermadec Islands. N Z J Mar Fresh 20:521–535. doi: 10.1080/00288330.1986.9516173 CrossRefGoogle Scholar
  47. Schiel DR, Lilley SA, South PM, Coggins JHJ (2016) Decadal changes in sea surface temperature, wave forces and intertidal structure in New Zealand. Mar Ecol Prog Ser 548:77–95. doi: 10.3354/meps11671 CrossRefGoogle Scholar
  48. Sewell MA, Young CM (1999) Temperature limits to fertilization and early development in the tropical sea urchin Echinometra lucunter. J Exp Mar Biol Ecol 236:291–305. doi: 10.1016/S0022-0981(98)00210-X CrossRefGoogle Scholar
  49. Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine “winners” and “losers”. J Exp Biol 213:912–920. doi: 10.1242/jeb.037473 CrossRefGoogle Scholar
  50. Sunday JM, Crim RN, Harley CDG, Hart MW (2011) Quantifying rates of evolutionary adaptation in response to ocean acidification. PLoS One 6:e22881. doi: 10.1371/journal.pone.0022881 CrossRefGoogle Scholar
  51. Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042. doi: 10.1242/dev.033183 CrossRefGoogle Scholar
  52. Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era—concepts and misconceptions. Nat Rev Genet 9:255–266. doi: 10.1038/nrg2322 CrossRefGoogle Scholar
  53. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  54. Willmer P (1999) Environmental physiology of animals. Blackwell Publisher, MassachusettsGoogle Scholar
  55. Zhang W, Zhao C, Chen M, Chang Y, Song J, Luo S (2013) Family growth response to different laboratory culture environments shows genotype-environment interaction in the sea urchin Strongylocentrotus intermedius. Aquac Res 44:1706–1714. doi: 10.1111/j.1365-2109.2012.03175.x Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  2. 2.Leigh Marine Laboratory, Institute of Marine ScienceUniversity of AucklandWarkworthNew Zealand

Personalised recommendations