Skip to main content
Log in

Environmentally induced morphological variation in the temperate reef fish, Forsterygion lapillum (F. Tripterygiidae)

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The study of phenotypic variation at the level of populations and species is central to understanding the processes that lead to evolutionary diversification. Triplefin fishes (Tripterygiidae) are a diverse and ecologically important family on New Zealand rocky reefs. This assemblage provides an opportunity to explore phenotype-environment relationships and the mechanisms responsible for the ecological speciation that is thought to have driven diversification in this clade. To test these relationships, we used two main approaches. Firstly, we used a geometric morphometric approach, and secondly, we used controlled rearing experiments in aquaria to examine the mechanism behind this phenotypic variation. The results showed that wild populations of the habitat generalist Forsterygion lapillum differed in body and fin morphology across a gradient in wave exposure in a region with extensive gene flow. Results of the tank experiments demonstrated that new recruits of F. lapillum from the same location that were raised in distinct water movement environments became morphologically distinct, whereas new recruits of F. lapillum from distinct water movement environments that were raised in identical conditions did not. The reciprocal rearing experiments, in conjunction with the morphological variation shown in wild individuals across the exposure gradient, indicate that plasticity is predominantly responsible for the phenotypic variation seen in F. lapillum populations in the Hauraki Gulf, New Zealand.

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

Access this article

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
Fig. 6

Similar content being viewed by others

Data availability

Data can be made available on request. There was no code used in this study.

References

  • Adams CE, Huntingford FA (2004) Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of Arctic charr. Biol J Linn Soc 81:611–618. https://doi.org/10.1111/j.1095-8312.2004.00314.x

    Article  Google Scholar 

  • Alberto FJ et al (2013) Potential for evolutionary responses to climate change evidence from tree populations. Glob Chang Biol 19:1645–1661. https://doi.org/10.1111/gcb.12181

    Article  PubMed  PubMed Central  Google Scholar 

  • Barluenga M, Stölting K, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719–723

    Article  CAS  PubMed  Google Scholar 

  • Bellwood DR, Wainwright PC, Fulton CJ, Hoey A (2002) Assembly rules and functional groups at global biogeographical scales. Funct Ecol 16:557–562. https://doi.org/10.1046/j.1365-2435.2002.00655.x

    Article  Google Scholar 

  • Binning SA, Roche DG (2015) Water flow and fin shape polymorphism in coral reef fishes. Ecology 96:828–839. https://doi.org/10.1890/14-0426.1

    Article  PubMed  Google Scholar 

  • Blake RW (1981) Influence of pectoral fin shape on thrust and drag in labriform locomotion. J Zool 194:53–66. https://doi.org/10.1111/j.1469-7998.1981.tb04578.x

    Article  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data. Geometry and biology. Cambridge University Press, England

    Google Scholar 

  • Bouton N, Witte F, Van Alphen JJM (2002) Experimental evidence for adaptive phenotypic plasticity in a rock-dwelling cichlid fish from Lake Victoria. Biol J Linn Soc 77:185–192

    Article  Google Scholar 

  • Bowen BB et al (2020) Species radiations in the sea: what the flock? J Hered 111:70–83. https://doi.org/10.1093/jhered/esz075

    Article  PubMed  Google Scholar 

  • Burrows MJ, Harvey R, Robb L (2008) Wave exposure indices from digital coastlines and the prediction of rocky shore community structure. Mar Ecol Prog Ser 353:1–12

    Article  Google Scholar 

  • Conlith AJ, Kidd MR, Kocher TD, Albertson RC (2020) Ecomorphological divergence and habitat lability in the context of robust patterns of modularity in the cichlid feeding apparatus. BMC Evol Biol 20:95

    Article  Google Scholar 

  • Connell SD, Jones GP (1991) The influence of habitat complexity on postrecruitment processes in a temperate reef fish population. J Exp Mar Bio Ecol 151:271–294. https://doi.org/10.1016/0022-0981(91)90129-k

    Article  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland

    Google Scholar 

  • Denny CM (2005) Distribution and abundance of labrids in northeastern New Zealand: the relationship between depth, exposure and pectoral fin ratio. Environ Biol Fishes 72:33–43

    Article  Google Scholar 

  • Denny MW (1988) Biology and the mechanics of the wave-swept environment. Princeton University Press, Princeton

    Book  Google Scholar 

  • Doak W (2003) A photographic guide to the fishes of New Zealand. New Holland, Auckland

    Google Scholar 

  • Doebeli M, Dieckmann U (2003) Speciation along environmental gradients. Nature 421:259–264

    Article  CAS  PubMed  Google Scholar 

  • Domenici P (2003) Habitat, body design and the swimming performance of fish. In: Bels VL, Gasc JP, Casinos A (eds) Vertebrate biomechanics and evolution, BIOS Scientific, Oxford, pp 137–160

  • Feary DA, Clements KD (2006) Habitat use by triplefin species (Tripterygiidae) on rocky reefs in New Zealand. J Fish Biol 69:1031–1046. https://doi.org/10.1111/j.1095-8649.2006.01179.x

    Article  Google Scholar 

  • Feary DA, Wellenreuther M, Clements KD (2009) Trophic ecology of New Zealand triplefin fishes (Family Tripterygiidae). Mar Biol 156:1703–1714. https://doi.org/10.1007/s00227-009-1205-2

    Article  Google Scholar 

  • Francis M (2013) Coastal fishes of New Zealand: identification, biology and behaviour. Craig Potton Publishing, Nelson

    Google Scholar 

  • Fulton CJ, Bellwood DR, Wainwright PC (2001) The relationship between swimming ability and habitat use in wrasses (Labridae). Mar Biol 139:25–33

    Article  Google Scholar 

  • Fulton CJ, Bellwood DR, Wainwright PC (2005) Wave energy and swimming performance shape coral reef fish assemblages. Proc Roy Soc B 272:827–832. https://doi.org/10.1098/rspb.2004.3029

    Article  CAS  Google Scholar 

  • Fulton CJ, Binning SA, Wainwright PC, Bellwood DR (2013) Wave-induced abiotic stress shapes phenotypic diversity in a coral reef fish across a geographical cline. Coral Reefs 32:685–689. https://doi.org/10.1007/s00338-013-1039-8

    Article  Google Scholar 

  • Fulton CJ, Wainwright PC, Hoey AS, Bellwood DR (2017) Global ecological success of Thalassoma fishes in extreme coral reef habitats. Ecol Evol 7:466–472. https://doi.org/10.1002/ece3.2624

    Article  PubMed  Google Scholar 

  • Gerstner CL, Webb PW (1998) The station-holding performance of the plaice Pleuronectes platessa on artificial substratum ripples. Can J Zool 76:260–268

    Article  Google Scholar 

  • Gillespie RG et al (2020) Comparing adaptive radiations across space, time, and taxa. J Hered 111:1–20

    Article  PubMed  PubMed Central  Google Scholar 

  • Gomes-Jr JL, Monteiro LR (2008) Morphological divergence patterns among populations of Poecilia vivipara (Teleostei; Poeciliidae): test of an ecomorphological paradigm. Biol J Linn Soc 93:799–812

    Article  Google Scholar 

  • Griffiths SP (2000) The use of clove oil as an anaesthetic and method for sampling intertidal rockpool fishes. J Fish Biol 57:1453–1464

    Article  Google Scholar 

  • Hickey AJR, Clements KD (2003) Key metabolic enzymes and muscle structure in triplefin fishes (Tripterygiidae): a phylogenetic comparison. J Comp Phys B 173:113–123. https://doi.org/10.1007/s00360-002-0313-9

    Article  CAS  Google Scholar 

  • Hickey AJR, Clements KD (2005) Genome size evolution in New Zealand triplefin fishes. J Hered 96:356–362. https://doi.org/10.1093/jhered/esi061

    Article  CAS  PubMed  Google Scholar 

  • Hickey AJR, Lavery SD, Hannan DA, Baker CS, Clements KD (2009) New Zealand triplefin fishes (family Tripterygiidae): contrasting population structure and mtDNA diversity within a marine species flock. Mol Ecol 18:680–696. https://doi.org/10.1111/j.1365-294X.2008.04052.x

    Article  CAS  PubMed  Google Scholar 

  • Higham TE, Stewart WJ, Wainwright PC (2015) Turbulence, temperature, and turbidity: the ecomechanics of predator–prey interactions in fishes. Integr Comp Biol 55:6–20

    Article  PubMed  Google Scholar 

  • Hilton Z, Wellenreuther M, Clements KD (2008) Physiology underpins habitat partitioning in a sympatric sister-species pair of intertidal fishes. Funct Ecol 22:1108–1117. https://doi.org/10.1111/j.1365-2435.2008.01465.x

    Article  Google Scholar 

  • Hulsey CD, Holzman R, Meyer A (2018) Dissecting a potential spandrel of adaptive radiation: body depth and pectoral fin ecomorphology coevolve in Lake Malawi cichlid fishes. Ecol Evol 8:11945–11953. https://doi.org/10.1002/ece3.4651

    Article  PubMed  PubMed Central  Google Scholar 

  • Kane EA, Higham TE (2012) Life in the flow lane: differences in pectoral fin morphology suggest transitions in station-holding demand across species of marine sculpin. Zoology 115:223–232. https://doi.org/10.1016/j.zool.2012.03.002

    Article  PubMed  Google Scholar 

  • Kaufmann J, Lenz TL, Kalbe M, Milinski M, Eizaguirre C (2017) A field reciprocal transplant experiment reveals asymmetric costs of migration between lake and river ecotypes of three-spined sticklebacks (Gasterosteus aculeatus). J Evol Biol 30:938–950. https://doi.org/10.1111/jeb.13057

    Article  CAS  PubMed  Google Scholar 

  • Keeley ER, Parkinson EA, Taylor EB (2007) The origins of ecotypic variation of rainbow trout: a test of environmental vs. genetically based differences in morphology. J Evol Biol 20:725–736

    Article  CAS  PubMed  Google Scholar 

  • Koehl MAR (1996) When does morphology matter? Ann Rev Ecol Evol Syst 27:501–542

    Article  Google Scholar 

  • Laland KN et al (2015) The extended evolutionary synthesis: its structure, assumptions and predictions. Proc Roy Soc B 282:20151019

    Article  Google Scholar 

  • Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446

    Article  PubMed  CAS  Google Scholar 

  • Langerhans RB, Reznick DN (2010) Ecology and evolution of swimming performance in fishes: predicting evolution. In: Domenici PG, Kapoor BG (eds) Fish locomotion: an eco-ethological perspective. Science Publishers, Enfield, pp 200–248

    Chapter  Google Scholar 

  • Losos JB, Warhelt KI, Schoener TW (1997) Adaptive differentiation following experimental island colonisation in Anolis lizards. Nature 387:70–73

    Article  CAS  Google Scholar 

  • Marcoux TM, Korsmeyer KE (2019) Energetics and behavior of coral reef fishes during oscillatory swimming in a simulated wave surge. J Exp Biol 222:1–12. https://doi.org/10.1242/jeb.191791

    Article  Google Scholar 

  • Martin CH, Richards EJ (2019) The paradox behind the pattern of rapid adaptive radiation: how can the speciation process sustain itself through and early burst? Ann Rev Ecol Evol Syst 50:569–593

    Article  Google Scholar 

  • Martin RA, Pfennig DW (2010) Field and experimental evidence that competition and ecological opportunity promote resource polymorphism. Biol J Linn Soc 100:73–88

    Article  Google Scholar 

  • McDermott CJ, Shima JS (2006) Ontogenetic shifts in microhabitat preference of the temperate reef fish Forsterygion lapillum: implications for population limitation. Mar Ecol Prog Ser 320:259–266. https://doi.org/10.3354/meps320259

    Article  Google Scholar 

  • Mendel G (1866) Versuche über Pflanzen-Hybriden [experiments on plant hybrids]. Verhandlungen Des Naturforschenden Vereines Abhandlungern Brünn 4:3–47

    Google Scholar 

  • Mensink PJ, Shima JS (2014) Patterns of co-occurrence and interactions between age classes of the common triplefin, Forsterygion lapillum. Mar Biol 161:1285–1298. https://doi.org/10.1007/s00227-014-2418-6

    Article  Google Scholar 

  • Montgomery JC, Macdonald JA (1984) Performance of motor systems in Antarctic fishes. J Comp Phys A 154:241–248

    Article  Google Scholar 

  • Muschick M, Barluenga M, Salzburger W, Meyer A (2011) Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol Biol. https://doi.org/10.1186/1471-2148-11-116

    Article  PubMed  PubMed Central  Google Scholar 

  • NIWA (2016) CliFlo historical wind data. Available at http://cliflo.niwa.co.nz/. Accessed Feb 2016

  • NOAA (2016) MetOcean wavewatch. Available at https://www.metocean.co.nz/. Accessed Feb 2016

  • Norton SF (1991) Capture success and diet of cottid fishes—the role of predator morphology and attack kinematics. Ecology 72:1807–1819

    Article  Google Scholar 

  • Nosil P (2012) Ecological speciation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Pepino M, Magnan P, Proulx R (2018) Field evidence for a rapid adaptive plastic response in morphology and growth of littoral and pelagic brook charr: a reciprocal transplant experiment. Funct Ecol 32:161–170. https://doi.org/10.1111/1365-2435.12929

    Article  Google Scholar 

  • Pfennig DW, Matthew A, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Tree 25:459–467

    PubMed  Google Scholar 

  • Rabone M, Lavery SD, Little A, Clements KD (2015) Discordance between nuclear and mitochondrial DNA analyses of population structure in closely related triplefin fishes (Forsterygion lapillum and F. capito, F. Tripterygiidae) supports speciation with gene flow. Mar Biol 162:1611–1624

    Article  CAS  Google Scholar 

  • Rajkov J, Weber AA-T, Salzburger W, Egger B (2018) Adaptive phenotypic plasticity contributes to divergence between lake and river populations of an east African cichlid fish. Ecol Evol 8:7323–7333

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson BW, Wilson DS, Margosian AS, Lotito PT (1993) Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evol Ecol 7:451–464

    Article  Google Scholar 

  • Rohlf FJ (2008) TPSDig. Software for geometric morphometric analyses. SUNY at Stony Brook NY. Available at http://life.bio.sunysb.edu/morph/. Accessed 10 Oct 2015

  • Schluter D (2000) The ecology of adaptive radiations. Oxford University Press, Oxford

    Google Scholar 

  • Shears NT, Babcock RC (2004) Community composition and structure of shallow subtidal reefs in northeastern New Zealand. Sci Conserv 245:1–22

    Google Scholar 

  • Sheets HD (2004) IMP. Software for geometric morphometric analysis, Canisius College, Buffalo NY. Available at http://www.canisius.edu/~sheets/morphsoft.html

  • Smith ANH, Duffy CAJ, Leathwick JR (2013) Predicting the distribution and relative abundance of fishes on shallow subtidal reefs around New Zealand. Sci Conserv 323:1–25

    Google Scholar 

  • Smith TB, Skúlason S (1996) Evolutionary significance of resource polymorphisms in fishes, amphibians and birds. Annu Rev Ecol Syst 27:111–133

    Article  Google Scholar 

  • Stewart AL, Clements KD (2015) Family Tripterygiidae. In: Stewart AL, Struthers CD (eds) The fishes of New Zealand, vol 4. Te Papa Press, Wellington, pp 1491–1523

    Google Scholar 

  • Stoks R, Geerts AN, De Meester L (2014) Evolutionary and plastic responses of freshwater invertebrates to climate change: realized patterns and future potential. Evol Appl 7:42–55. https://doi.org/10.1111/eva.12108

    Article  PubMed  Google Scholar 

  • Syms C (1995) Multiscale analysis of habitat association in a guild of blennioid fishes. Mar Ecol Prog Ser 125:31–43. https://doi.org/10.3354/meps125031

    Article  Google Scholar 

  • Taylor EB, McPhail JD (1985) Variation in burst and prolonged swimming performance among British Columbia populations of coho salmon, Oncorhynchus kisutch. Can J Fish Aq Sci 42:2029–2033

    Article  Google Scholar 

  • Thomas MLH (1986) A physically derived exposure index for marine shorelines. Ophelia 25:1–13

    Article  Google Scholar 

  • Thompson SM, Jones GP (1983) Interspecific territoriality and competition for food between the reef fishes Forsterygion varium and Pseudolabrus celidotus. Mar Biol 76:95–104. https://doi.org/10.1007/bf00393060

    Article  Google Scholar 

  • Tougeron K, van Baaren J, Llopis S, Ridel A, Doyon J, Brodeur J, Le Lann C (2018) Disentangling plasticity from local adaptation in diapause expression in parasitoid wasps from contrasting thermal environments: a reciprocal translocation experiment. Biol J Linn Soc 124:756–764. https://doi.org/10.1093/biolinnean/bly079

    Article  Google Scholar 

  • Videler JJ (1993) Fish swimming. Springer, New York

    Book  Google Scholar 

  • Walker JA, Westneat MW (2002a) Kinematics, dynamics, and energetics of rowing and flapping propulsion in fishes. Integr Comp Biochem Phys A 42:1032–1043. https://doi.org/10.1093/icb/42.5.1032

    Article  Google Scholar 

  • Walker JA, Westneat MW (2002b) Performance limits of labriform propulsion and correlates with fin shape and motion. J Exp Biol 205:177–187

    Article  PubMed  Google Scholar 

  • Webb PW (1994) The biology of fish swimming. In: Maddock L, Bone Q, Rayner JMV (eds) Mechanics and physiology of animal swimming. Cambridge University Press, Cambridge, pp 45–62

    Chapter  Google Scholar 

  • Webb PW, Gerstner CL, Minton ST (1996) Station-holding by the mottled sculpin, Cottus bairdi (Teleostei: Cottidae), and other fishes. Copeia 2:488–493

    Article  Google Scholar 

  • Webster MM, Atton N, Hart PJB, Ward AJW (2011) Habitat-specific morphological variation among threespine sticklebacks (Gasterosteus aculeatus) within a drainage basin. PLoS ONE 6:e21060. https://doi.org/10.1371/journal.pone.0021060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellenreuther M, Barrett PT, Clements KD (2007) Ecological diversification in habitat use by subtidal triplefin fishes (Tripterygiidae). Mar Ecol Prog Ser 330:235–246. https://doi.org/10.3354/meps330235

    Article  Google Scholar 

  • Wellenreuther M, Clements KD (2008) Determinants of habitat association in a sympatric clade of marine fishes. Mar Biol 154:393–402. https://doi.org/10.1007/s00227-008-0940-0

    Article  Google Scholar 

  • Wellenreuther M, Barrett PT, Clements KD (2009) The evolution of habitat specialisation in a group of marine triplefin fishes. Evol Ecol 23:557–568. https://doi.org/10.1007/s10682-008-9255-3

    Article  Google Scholar 

  • West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278. https://doi.org/10.1146/annurev.es.20.110189.001341

    Article  Google Scholar 

  • Wimberger PH (1994) Trophic polymorphisms, plasticity and speciation in vertebrates. In: Fresh KL, Fresh RJ (eds) Theory and application in fish feeding ecology. University of South Carolina Press, Colombia, pp 19–43

    Google Scholar 

  • Winkler NS, Paz-Goicoechea M, Lamb RW, Perez-Matus A (2017) Diet reveals links between morphology and foraging in a cryptic temperate reef fish. Ecol Evol 7:11124–11134

    Article  PubMed  PubMed Central  Google Scholar 

  • Yee WL, Sheets HD, Chapman PS (2011) Analysis of surstylus and aculeus shape and size using geometric morphometrics to discriminate Rhagoletis pomonella and Rhagoletis zephyria (Diptera: Tephritidae). Ann Entomol Soc Am 104:105–114

    Article  Google Scholar 

  • Zelditch ML, Swiderski DL, Sheets HD (2012) Geometric morphometrics for biologists: a primer, 2nd edn. Elsevier Academic Press, Amsterdam

    Google Scholar 

Download references

Acknowledgements

We thank Brady Doak for skippering the R. V. Hawere. We thank Evan Brown, Peter Browne, Brady Doak, Arie Spyksma and Jenni Stanley for assistance with specimen collection, Lauren Shea for lab assistance, Viv Ward for the fish graphics, and Ian McLeod for valuable conversations. We thank James Rohlf for useful conversations on allometry, and David Sheets for assistance with geometric morphometric analyses. We are also grateful to the staff and students at the Leigh Marine Laboratory. We thank the reviewers for their valuable remarks and suggestions that contributed to improving this manuscript. We thank E. Villouta for providing access to his Fetch Effect Analysis software.

Funding

PEC was funded by a University of Auckland Faculty of Science Doctoral Scholarship, a Faculty of Science internal research grant, and the Hutton Fund grant.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study's conception and design. Material preparation, data collection and analysis were performed by PC and CC. The first draft of the manuscript was written by PC and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Paul E. Caiger.

Ethics declarations

Conflict of interest

The authors have no conflict of interest.

Ethical approval

All work was undertaken in accordance with the University of Auckland Animal Ethics Committee approval 001047.

Additional information

Responsible Editor: D. Goulet.

Publisher's Note

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

Reviewed by undisclosed experts.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 544 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Caiger, P.E., Croq, C. & Clements, K.D. Environmentally induced morphological variation in the temperate reef fish, Forsterygion lapillum (F. Tripterygiidae). Mar Biol 168, 131 (2021). https://doi.org/10.1007/s00227-021-03939-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-021-03939-3

Navigation