Skip to main content
SpringerLink
Log in

Correlational selection on size and development time is inconsistent across early life stages

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Size and development time are universally important traits. Yet evolutionary trends in development time are often viewed as allometric and physiological by-products of initial size, when life-history theory predicts that both traits are targets of selection and evolve adaptively through opposing effects on fitness. Surprisingly, this prediction has rarely been tested by disentangling the direct and indirect effects of size and development time on fitness, as necessary to understand selection on each trait. Here, in a marine external fertiliser that provides novel scope for such tests, we measure directional, quadratic, and correlational selection acting on early size (of embryos and post-hatch larvae) and development time (from fertilisation to hatching) through survival of juveniles in the field. We find little directional selection acting on traits during this selective episode. Rather, selection is primarily correlational, targeting combinations of development time and post-development size in a way that acts against their already-weak positive correlation, and could eventually drive a negative correlation between them if persistent enough. Lack of correlational selection on combinations of embryo size and development time, in contrast, suggests that physiological or allometric constraints more likely explain their positive association. Hence, neither life-history theory nor principles of allometry and physiology alone may predict the evolution of size and development time, warranting greater appreciation of the tension between adaptive and non-adaptive explanations for evolutionary trends in these traits.

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

Similar content being viewed by others

Data availability

Data deposited on figshare (https://doi.org/10.6084/m9.figshare.12846710).

References

  • Arendt JD (1997) Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol 722:149–177

    Google Scholar 

  • Arnold SJ, Pfrender ME, Jones AG (2001) The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112:9–32

    PubMed  Google Scholar 

  • Arnold PA, Nicotra AB, Kruuk LEB (2019) Sparse evidence for selection on phenotypic plasticity in response to temperature. Philos Trans R Soc B 3741768:20180185

    Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 671:48

    Google Scholar 

  • Blanckenhorn WU (2000) The evolution of body size: what keeps organisms small? Q Rev Biol 754:385–407

    Google Scholar 

  • Blows MW (2007) A tale of two matrices: multivariate approaches in evolutionary biology. J Evol Biol 201:1–8

    Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 243:127–135

    Google Scholar 

  • Bonnet T, Wandeler P, Camenisch G, Postma E (2017) Bigger is fitter? Quantitative genetic decomposition of selection reveals an adaptive evolutionary decline of body mass in a wild rodent population. PLoS Biol 151:e1002592

    Google Scholar 

  • Brodie ED (1992) Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 465:1284–1298

    Google Scholar 

  • Brodie ED, Moore AJ, Janzen FJ (1995) Visualizing and quantifying natural selection. Trends Ecol Evol 108:313–318

    Google Scholar 

  • Cameron H, Monro K, Malerba M, Munch S, Marshall D (2016) Why do larger mothers produce larger offspring? A test of classic theory. Ecology 9712:3452–3459

    Google Scholar 

  • Chippindale AK, Alipaz JA, Chen HW, Rose MR (1997) Experimental evolution of accelerated development in Drosophila. 1. Developmental speed and larval survival. Evolution 515:1536–1551

    Google Scholar 

  • Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2017) The other 96%: can neglected sources of fitness variation offer new insights into adaptation to global change? Evol Appl 103:267–275

    Google Scholar 

  • Chirgwin E, Marshall Dustin J, Sgrò Carla M, Monro K (2018) How does parental environment influence the potential for adaptation to global change? Proc R Soc B Biol Sci 2851886:20181374

    Google Scholar 

  • Chirgwin E, Marshall DJ, Monro K (2020) Physical and physiological impacts of ocean warming alter phenotypic selection on sperm morphology. Funct Ecol 343:646–657

    Google Scholar 

  • Church SH, Donoughe S, de Medeiros BAS, Extavour CG (2019) Insect egg size and shape evolve with ecology but not developmental rate. Nature 5717763:58–62

    Google Scholar 

  • Crean AJ, Monro K, Marshall DJ (2011) Fitness consequences of larval traits persist across the metamorphic boundary. Evolution 6511:3079–3089

    Google Scholar 

  • CSIRO (2016) CSIRO marine and atmopsheric research. http://www.cmar.csiro.au. Accessed 2 Sept 2016

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 861:97–116

    Google Scholar 

  • Eck DJ, Shaw RG, Geyer CJ, Kingsolver JG (2015) An integrated analysis of phenotypic selection on insect body size and development time. Evolution 699:2525–2532

    Google Scholar 

  • Elston DA, Moss R, Boulinier T, Arrowsmith C, Lambin X (2001) Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122:563–569

    CAS  PubMed  Google Scholar 

  • Ficetola GF, De Bernardi F (2006) Trade-off between larval development rate and post-metamorphic traits in the frog Rana latastei. Evol Ecol 202:143–158

    Google Scholar 

  • Foo SA, Byrne M (2016) Chapter 2: Acclimatization and adaptive capacity of marine species in a changing ocean. In: Curry BE (ed) Advances in marine biology, vol 74. Academic Press, Cambridge, pp 69–116

    Google Scholar 

  • Futuyma DJ (2010) Evolutionary constraint and ecological consequences. Evolution 647:1865–1884

    Google Scholar 

  • Gillooly JF (2000) Effect of body size and temperature on generation time in zooplankton. J Plankton Res 222:241–251

    Google Scholar 

  • Gillooly JF, Charnov EL, West GB, Savage VM, Brown JH (2002) Effects of size and temperature on developmental time. Nature 4176884:70–73

    Google Scholar 

  • Hinegardner RT (1975) Morphology and genetics of sea-urchin development. Am Zool 153:679–689

    Google Scholar 

  • Hirst A, Lopez-Urrutia A (2006) Effects of evolution on egg development time. Mar Ecol Prog Ser 326:29–35

    Google Scholar 

  • Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301

    Google Scholar 

  • Janzen FJ, Stern HS (1998) Logistic regression for empirical studies of multivariate selection. Evolution 526:1564–1571

    Google Scholar 

  • Karr TL, Mittenthal JE (1992) Adaptive mechanisms that accelerate embryonic development in Drosophila. In: Mittenthal JE, Baskin AB (eds) Principles of organization in organisms. Westview Press, Boulder

    Google Scholar 

  • Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 102:251–268

    Google Scholar 

  • Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of Cope’s rule of phyletic size increase. Evolution 587:1608–1612

    Google Scholar 

  • Kingsolver JG, Smith SG (1995) Estimating selection on quantitative traits using capture-recapture data. Evolution 492:384–388

    Google Scholar 

  • Kingsolver JG, Diamond SE, Seiter SA, Higgins JK (2012a) Direct and indirect phenotypic selection on developmental trajectories in Manduca sexta. Funct Ecol 263:598–607

    Google Scholar 

  • Kingsolver JG, Diamond SE, Siepielski AM, Carlson SM (2012b) Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol Ecol 265:1101–1118

    Google Scholar 

  • Lambert CC (2005) Historical introduction, overview, and reproductive biology of the protochordates. Can J Zool 831:1–7

    Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 376:1210–1226

    Google Scholar 

  • Levitan DR, Sewell MA, Chia FS (1991) Kinetics of fertilization in the sea urchin Strongylocentrotus franciscanus: interaction of gamete dilution, age, and contact time. Biol Bull 1813:371–378

    Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and the analysis of quantitative traits. Sinauer, Sunderland

    Google Scholar 

  • Manly B (1985) The statistics of natural selection on animal populations. Chapman and Hall, London

    Google Scholar 

  • Marshall DJ, Bolton TF (2007) Effects of egg size on the development time of non-feeding larvae. Biol Bull 2121:6–11

    Google Scholar 

  • Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. In: Sims DW (ed) Advances in Marine Biology, vol 53. Elsevier Academic Press Inc, San Diego, pp 1–60

    Google Scholar 

  • Marshall DJ, Morgan SG (2011) Ecological and evolutionary consequences of linked life-history stages in the sea. Curr Biol 2118:R718–R725

    Google Scholar 

  • Marshall DJ, Pettersen AK, Cameron H (2018) A global synthesis of offspring size variation, its eco-evolutionary causes and consequences. Funct Ecol 326:1436–1446

    Google Scholar 

  • Marshall DJ, Pettersen AK, Bode M, White CR (2020) Developmental cost theory predicts thermal environment and vulnerability to global warming. Nat Ecol Evol 43:406–411

    Google Scholar 

  • McLaren IA (1965) Some relationships between temperature and egg size, body size, development rate, and fecundity, of the copepod Pseudocalanus. Limnol Oceanogr 104:528–538

    Google Scholar 

  • Mojica JP, Kelly JK (2010) Viability selection prior to trait expression is an essential component of natural selection. Proc R Soc B 2771696:2945–2950

    Google Scholar 

  • Monro K, Marshall DJ (2014) Faster is not always better: selection on growth rate fluctuates across life history and environments. Am Nat 1836:798–809

    Google Scholar 

  • Monro K, Marshall DJ (2015) The biogeography of fertilization mode in the sea. Glob Ecol Biogeogr 2412:1499–1509

    Google Scholar 

  • Morgan SG (1995) Life and death in the plankton: larval mortality and adaptation. CRC Press, Boca Raton

    Google Scholar 

  • Pauly D, Pullin RSV (1988) Hatching time in spherical, pelagic, marine fish eggs in response to temperature and egg size. Environ Biol Fishes 224:261–271

    Google Scholar 

  • Pettersen AK, White CR, Marshall DJ (2015) Why does offspring size affect performance?. Integrating metabolic scaling with life-history theory, Proc R Soc B, p 2821819

    Google Scholar 

  • Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2018) Does the cost of development scale allometrically with offspring size? Funct Ecol 323:762–772

    Google Scholar 

  • Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2019) Linking life-history theory and metabolic theory explains the offspring size-temperature relationship. Ecol Lett 223:518–526

    Google Scholar 

  • Phillips PC, Arnold SJ (1989) Visualizing multivariate selection. Evolution 436:1209–1222

    Google Scholar 

  • Rius M, Turon X, Dias GM, Marshall DJ (2010) Propagule size effects across multiple life-history stages in a marine invertebrate. Funct Ecol 243:685–693

    Google Scholar 

  • Rius M, Teske PR, Manriquez PH, Suarez-Jimenez R, McQuaid CD, Castilla JC (2017) Ecological dominance along rocky shores, with a focus on intertidal ascidians. In: Hawkins SJ, Evans AJ, Dale AC, Firth LB, Hughes DJ, Smith IP (eds) Oceanography and marine biology: an annual review, vol 55. CRC Press-Taylor & Francis Group, Boca Raton, pp 55–85

    Google Scholar 

  • SAS Institute (2015) SAS/STAT® 14.1 User’s Guide. Retrieved from North Carolina

  • Schluter D, Price TD, Rowe L (1991) Conflicting selection pressures and life-history trade-offs. Proc R Soc B 2461315:11–17

    Google Scholar 

  • Semmens D, Swearer SE (2011) Extended incubation affects larval morphology, hatching success and starvation resistance in a terrestrially spawning fish, Galaxias maculatus (Jenyns 1842). J Fish Biol 794:980–990

    Google Scholar 

  • Sibly R, Calow P, Nichols N (1985) Are patterns of growth adaptive? J Theor Biol 1123:553–574

    Google Scholar 

  • Siepielski AM, Morrissey MB, Carlson SM, Francis CD, Kingsolver JG, Whitney KD, Kruuk LEB (2019) No evidence that warmer temperatures are associated with selection for smaller body sizes. Proc R Soc B 2861907:20191332

    Google Scholar 

  • Sinervo B, McEdward LR (1988) Developmental consequences of an evolutionary change in egg size: an experimental test. Evolution 425:885–899

    Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Strathmann RR, Staver JM, Hoffman JR (2002) Risk and the evolution of cell-cycle durations of embryos. Evolution 564:708–720

    Google Scholar 

  • R Core Team (2019) A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/. Accessed 7 Oct 2019

  • Troth A, Puzey JR, Kim RS, Willis JH, Kelly JK (2018) Selective trade-offs maintain alleles underpinning complex trait variation in plants. Science 3616401:475

    Google Scholar 

  • Walsh B, Blows MW (2009) Abundant genetic variation plus strong selection = multivariate genetic constraints: a geometric view of adaptation. Annu Rev Ecol Evol Syst 40:41–59

    Google Scholar 

  • Walsh B, Lynch M (2018) Evolution and selection of quantitative traits. Oxford University Press, Oxford

    Google Scholar 

Download references

Acknowledgements

We are grateful to the Blairgowrie Yacht Squadron for access to our field sites. We thank Dustin Marshall and Carla Sgrò for insightful discussions and comments on early versions of the manuscript, and Allison Chirgwin, Neil Chirgwin, and Laura Rigby for help collecting data. We also thank two anonymous reviewers and the Associate Editor for helpful advice that greatly improved our manuscript.

Funding

Funding was provided by grants and fellowships awarded under the Australian Research Council’s Discovery Scheme.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Monash University, Melbourne, VIC, Australia

    Evatt Chirgwin & Keyne Monro

Authors
  1. Evatt Chirgwin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Keyne Monro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Evatt Chirgwin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (CSV 9 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chirgwin, E., Monro, K. Correlational selection on size and development time is inconsistent across early life stages. Evol Ecol 34, 681–691 (2020). https://doi.org/10.1007/s10682-020-10065-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-020-10065-x

Keywords

Search

Navigation