[en] The iterative nature of ecomorphological diversification is observed in various groups of animals. However, studies explicitly testing the consistency of morphological variation across and within species are scarce. Antarctic notothenioids represent a textbook example of adaptive radiation in marine fishes. Within Nototheniidae, the endemic Antarctic genus Trematomus consists of 15 extant species, some with documented large intraspecific variability. Here, we quantify head shape disparity in 11 species of Trematomus by landmark-based geometric morphometrics, and we illustrate repeated events of divergence and convergence of their head morphology. Taking advantage of the polymorphism observed in some species of Trematomus, we also show that two closely related species or clades (e.g., Trematomus bernacchii and T. hansoni) are characterised by the same level of morphological disparity as observed at the level of the entire genus. Interestingly, the same main axes of shape variation are shared between and within species, indicating repeated morphological diversification. Overall, we illustrate a similarity of intra- and interspecific patterns of phenotypic diversity providing new insights into the mechanisms that underlie the diversification of Antarctic fishes.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Adams D.C. & Otárola-Castillo E. (2013). Geomorph: An r package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution 4: 393–399. https://doi.org/10.1111/2041-210X.12035
Adams D.C., Rohlf F.J. & Slice D.E. (2013). A field comes of age: Geometric morphometrics in the 21st century. Hystrix 24 (1): 7–14.
Aguilar-Medrano R., Frédérich B., de Luna E. & Balart E.F. (2011). Patterns of morphological evolution of the cephalic region in damselfishes (Perciformes: Pomacentridae) of the Eastern Pacific. Biological Journal of the Linnean Society 102(3): 593–613. https://doi.org/10.1111/j.1095-8312.2010.01586.x
Aguilar-Medrano R., Frédérich B., Balart E.F. & de Luna E. (2013). Diversification of the pectoral fin shape in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific. Zoomorphology 132: 197–213. https://doi.org/10.1007/s00435-012-0178-8
Alfaro M.E., Santini F. & Brock C.D. (2007). Do reefs drive diversification in marine teleosts? Evidence from the pufferfish and their allies (order Tetraodontiformes). Evolution 61: 2104–2126. https://doi.org/10.1111/j.1558-5646.2007.00182.x
Bernardi G. & Goswami U. (1997). Molecular evidence for cryptic species among the Antarctic fish Trematomus bernacchii and Trematomus hansoni. Antarctic Science 9: 381–385. https://doi.org/10.1017/S0954102097000485
Bookstein F. (1991). Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press.
Brenner M., Buck B.H., Cordes S., Dietrich L., Jacob U., Mintenbeck K., Schröder A., Brey T., Knust R. & Arntz W. (2001). The role of iceberg scours in niche separation within the Antarctic fish genus Trematomus. Polar Biology 24: 502–507. https://doi.org/10.1007/s003000100246
Burbrink F.T., Chen X., Myers E.A., Brandley M.C. & Pyron R.A. (2012). Evidence for determinism in species diversification and contingency in phenotypic evolution during adaptive radiation. Proceedings of the Royal Society B: Biological Sciences 279: 4817–4826. https://doi.org/10.1098/rspb.2012.1669
Casaux R. & Barrera-Oro E. (2013). Dietary overlap in inshore notothenioid fish from the Danco Coast, Western Antarctic Peninsula. Polar Research 32. https://doi.org/10.3402/polar.v32i0.21319
Causse R., Ozouf-Costaz C., Koubbi P., Lamy D., Eléaume M., Dettaï A., Duhamel G., Busson F., Pruvost P., Post A., Beaman R.J. & Riddle M.J. (2011) Demersal ichthyofaunal shelf communities from the Dumont d’Urville Sea (East Antarctica). Polar Science 5: 272–285. https://doi.org/10.1016/j.polar.2011.03.004
Collar D.C., Reece J.S., Alfaro M.E., Wainwright P.C. & Mehta R.S. (2014). Imperfect morphological convergence: Variable changes in cranial structures underlie transitions to durophagy in moray eels. American Naturalist 183 (6): E168–E184. https://doi.org/10.1086/675810
Collyer M.L., Sekora D.J. & Adams D.C. (2015). A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 115: 357–365. https://doi.org/10.1038/hdy.2014.75
Cooper W.J., Parsons K., McIntyre A., Kern B., McGee-Moore A. & Albertson R.C. (2010). Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within african rift-lakes. PLoS ONE 5: A38–A50. https://doi.org/10.1371/journal.pone.0009551
De Meyer J., Christiaens J. &Adriaens D. (2016). Diet-induced phenotypic plasticity in European eel (Anguilla anguilla). Journal of Experimental Biology 219: 354–363. https://doi.org/10.1242/jeb.131714
Dornburg A., Sidlauskas B., Santini F., Sorenson L., Near T.J. & Alfaro M.E. (2011). The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (family: Balistidae). Evolution 65: 1912–1926. https://doi.org/10.1111/j.1558-5646.2011.01275.x
Dornburg A., Federman S., Lamb A.D., Jones C.D. & Near T.J. (2017). Cradles and museums of Antarctic teleost biodiversity. Nature Ecology and Evolution 1: 1379–1384. https://doi.org/10.1038/s41559-017-0239-y
Duhamel G., Hulley P.-A., Causse R., Koubbi P., Vacchi M., Pruvost P., Vigetta S., Irisson J.-O., Mormède S., Belchier M., Dettai A., Detrich H.W., Gutt J., Jones C.D., Kock K.-H., Lopez Abellan L.J., Van de Putte A.P. (2014). Chapter 7. Biogeographic patterns of fish. In: de Broyer C. et al. (eds) Biogeographic Atlas of the Southern Ocean: 328–362. Scientific Committee on Antarctic Research, Cambridge.
Eastman J.T. (2005). The nature of the diversity of Antarctic fishes. Polar Biology 28: 93–107. https://doi.org/10.1007/s00300-004-0667-4
Eastman J.T. (2019). An analysis of maximum body size and designation of size categories for notothenioid fishes. Polar Biology 42: 1131–1145. https://doi.org/10.1007/s00300-019-02502-7
Eastman J.T. & Barrera-Oro E. (2010). Buoyancy studies of three morphs of the Antarctic fish Trematomus newnesi (Nototheniidae) from the South Shetland Islands. Polar Biology 33: 823–831. https://doi.org/10.1007/s00300-009-0760-9
Eastman J.T. & DeVries A.L. (1985). Adaptations for cryopelagic life in the antarctic notothenioid fish Pagothenia borchgrevinki. Polar Biology 4: 45–52. https://doi.org/10.1007/BF00286816
Eastman J.T. & DeVries A.L. (1997). Biology and phenotypic plasticity of the Antarctic nototheniid fish Trematomus newnesi in McMurdo Sound. Antarctic Science 9: 27–35. https://doi.org/10.1017/S0954102097000047
Eastman J.T. & Eakin R.R. (2021). Checklist of the species of notothenioid fishes. Antarctic Science 33: 273–280. https://doi.org/10.1017/S0954102020000632
Ekau W. (1991). Morphological adaptations and mode of life in high antarctic fish. In: Di Prisco G., Maresca B. & Tota B. (eds) Biology of Antarctic Fish: 23–39. Springer, Berlin, Heidelberg.
Felsenstein J. (1985). Phylogenies and the comparative method. American Naturalist 125 (1): 1–15.
Frédérich B. & Sheets H.D. (2010). Evolution of ontogenetic allometry shaping giant species: A case study from the damselfish genus Dascyllus (Pomacentridae). Biological Journal of the Linnean Society 99 (1): 99–117. https://doi.org/10.1111/j.1095-8312.2009.01336.x
Frédérich B. & Vandewalle P. (2011). Bipartite life cycle of coral reef fishes promotes increasing shape disparity of the head skeleton during ontogeny: An example from damselfishes (Pomacentridae). BMC Evolutionary Biology 11: 82. https://doi.org/10.1186/1471-2148-11-82
Frédérich B., Sorenson L., Santini F., Slater G.J. & Alfaro M.E. (2013). Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). American Naturalist 181(1): 94–113. https://doi.org/10.1086/668599
Frédérich B., Cooper W.J. & Aguilar-Medrano R. (2016a). Ecomorphology and iterative ecological radiation of damselfishes. In: Frédérich B. & PArmentier E. (eds) Biology of Damselfishes: 183–203. CRC Press, Boca Raton.
Frédérich B., Marramà G., Carnevale G. & Santini F. (2016b). Non-reef environments impact the diversification of extant jacks, remoras and allies (Carangoidei, Percomorpha). Proceedings of the Royal Society B: Biological Sciences 283: 20161556. https://doi.org/10.1098/rspb.2016.1556
Frédérich B., Santini F., Konow N., Schnitzler J., Lecchini D. & Alfaro M.E. (2017). Body shape convergence driven by small size optimum in marine angelfishes. Biology Letters 13: 20170154. https://doi.org/10.1098/rsbl.2017.0154
Gajdzik L., Parmentier E., Michel L.N., Sturaro N., Soong K., Lepoint G. & Frédérich B. (2018). Similar levels of trophic and functional diversity within damselfish assemblages across Indo-Pacific coral reefs. Functional Ecology 32 (5): 1358–1369. https://doi.org/10.1111/1365-2435.13076
Gajdzik L., Aguilar-Medrano R. & Frédérich B. (2019). Diversification and functional evolution of reef fish feeding guilds. Ecology Letters 22 (4): 572–582. https://doi.org/10.1111/ele.13219
Hu Y., Ghigliotti L., Vacchi M., Pisano E., Detrich H.W. & Albertson R.C. (2016). Evolution in an extreme environment: Developmental biases and phenotypic integration in the adaptive radiation of antarctic notothenioids. BMC Evolutionary Biology 16: 142. https://doi.org/10.1186/s12862-016-0704-2
Klingenberg C.P. (1998). Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biological Reviews 73: 79–123.
Klingenberg C.P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology Evolution and Systematics 39: 115–132. https://doi.org/10.1146/annurev.ecolsys.37.091305.110054
Klingenberg C.P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources 11: 353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
Klingenberg C.P. & Ekau W. (1996). A combined, morphometric and phylogenetic analysis of an ecomorphological trend: Pelagization in antarctic fishes (Perciformes: Nototheniidae). Biological Journal of the Linnean Society 59: 143–177. https://doi.org/10.1111/j.1095-8312.1996.tb01459.x
Kock K.H., Barrera-Oro E., Belchier M., Collins M.A., Duhamel G., Hanchet S., Pshenichnov L., Welsford D. & Williams R. (2012). The role of fish as predators of krill (Euphausia superba) and other pelagic resources in the Southern Ocean. CCAMLR Science 19: 115–169.
La Mesa M., Dalú M. & Vacchi M. (2004). Trophic ecology of the emerald notothen Trematomus bernacchii (Pisces, Nototheniidae) from Terra Nova Bay, Ross Sea, Antarctica. Polar Biology 27: 721– 728. https://doi.org/10.1007/s00300-004-0645-x
Lannoo M.J. & Eastman J.T. (2000). Nervous and sensory system correlates of an epibenthic evolutionary radiation in Antarctic notothenioid fishes, genus Trematomus (Perciformes; Nototheniidae). Journal of Morphology 245: 67–79. https://doi.org/c6998x
Lautredou A.C., Bonillo C., Denys G., Cruaud C., Ozouf-Costaz C., Lecointre G. & Dettai A. (2010). Molecular taxonomy and identification within the Antarctic genus Trematomus (Notothenioidei, Teleostei): How valuable is barcoding with COI? Polar Science 4: 333–352. https://doi.org/10.1016/j.polar.2010.04.006
Litsios G., Sims C.A., Wüest R.O., Pearman P.B., Zimmermann N.E. & Salamin N. (2012). Mutualism with sea anemones triggered the adaptive radiation of clownfishes. BMC Evolutionary Biology 12: 212. https://doi.org/10.1186/1471-2148-12-212
Liu S.-Y.V., Frédérich B., Lavoué S., Chang J., Erdmann M.V., Mahardika G.N. & Barber P.H. (2018). Buccal venom gland associates with increased of diversification rate in the fang blenny fish Meiacanthus (Blenniidae; Teleostei). Molecular Phylogenetics and Evolution 125: 138–146. https://doi.org/10.1016/j.ympev.2018.03.027
Losos J.B., Jackman T.R., Larson A., de Queiroz K. & Rodriguez-Schettino L. (1998). Contingency and determinism in replicated adaptive radiations of island lizards. Science 279: 2115– 2118. https://doi.org/10.1126/science.279.5359.2115
Mahler D.L., Ingram T., Revell L.J. & Losos J.B. (2013). Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science 341: 292–295. https://doi.org/10.1126/science.1232392
Matschiner M., Hanel R. & Salzburger W. (2011). On the origin and trigger of the notothenioid adaptive radiation. PLoS ONE 6(4): e18911. https://doi.org/10.1371/journal.pone.0018911
MeloD., GarciaG., HubbeA.,AssisA.P. &MarroigG. (2016). EvolQG-An R package for evolutionary quantitative genetics. F1000Research 4: 925. https://doi.org/10.12688/F1000RESEARCH.7082.2
Meyer A. (1990). Morphometrics and allometry in the trophically polymorphic cichlid fish, Cichlasoma citrinellum: Alternative adaptations and ontogenetic changes in shape. Journal of Zoology 221(2): 237– 260. https://doi.org/10.1111/j.1469-7998.1990.tb03994.x
Moreira E., Juáres M. & Barrera-Oro E. (2014). Dietary overlap among early juvenile stages in an Antarctic notothenioid fish assemblage at Potter Cove, South Shetland Islands. Polar Biology 37: 1507–1515. https://doi.org/10.1007/s00300-014-1545-3
Muschick M., Indermaur A. & Salzburger W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology 22: 2362–2368. https://doi.org/10.1016/j.cub.2012.10.048
Near T.J., Dornburg A., Kuhn K.L., Eastman J.T., Pennington J.N., Patarnello T., Zane L., Fernández D.A. & Jones C.D. (2012). Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proceedings of the National Academy of Sciences of the United States of America 109: 3434–3439. https://doi.org/10.1073/pnas.1115169109
Near T.J., MacGuigan D.J., Parker E., Struthers C.D., Jones C.D. & Dornburg A. (2018). Phylogenetic analysis of Antarctic notothenioids illuminates the utility of RADseq for resolving Cenozoic adaptive radiations. Molecular Phylogenetics and Evolution 129: 268–279. https://doi.org/10.1016/j.ympev.2018.09.001
Pakhomov E.A. (1998). Feeding plasticity of the Antarctic fish Trematomus hansoni Boulenger, 1902 (Pisces: Nototheniidae): the influence of fishery waste on the diet. Polar Biology 19: 289–292. https://doi.org/10.1007/s003000050248
Parker E., Zapfe K.L., Yadav J., Frédérich B., Jones C.D., Economo E.P., Federman S., Near T.J. & Dornburg A. (2022). Periodic environmental disturbance drives repeated ecomorphological diversification in an adaptive radiation of antarctic fishes. bioRxiv 487509. [accessed 8 April 2022]. https://doi.org/10.1101/2022.04.08.487509
Pfennig D.W., McGee M. (2010). Resource polyphenism increases species richness: A test of the hypothesis. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 577–591. https://doi.org/10.1098/rstb.2009.0244
Pfennig D.W., Wund M.A., Snell-Rood E.C., Cruickshank T., Schlichting C.D. & Moczek A.P. (2010). Phenotypic plasticity’s impacts on diversification and speciation. Trends in Ecology and Evolution 25: 459–467. https://doi.org/10.1016/j.tree.2010.05.006
Piacentino G.L.M. & Barrera-Oro E. (2009). Phenotypic plasticity in the Antarctic fish Trematomus newnesi (Nototheniidae) from the South Shetland Islands. Polar Biology 32: 1407–1413. https://doi.org/10.1007/s00300-009-0651-0
Revell L.J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3: 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rohlf F.J. (2004). TpsDig2, a software program for landmark data acquisition. Available at www.sbmorphometrics.org.
Rohlf F.J. & Slice D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39: 40–59. https://doi.org/10.2307/2992207
Rolland J., Silvestro D., Litsios G., Faye L. & Salamin N. (2018). Clownfishes evolution below and above the species level. Proceedings of the Royal Society B: Biological Sciences 285: 20171796. https://doi.org/10.1098/rspb.2017.1796
Ruber L. & Adams D.C. (2001). Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika. Journal of Evolutionary Biology 14: 325–332. https://doi.org/10.1046/j.1420-9101.2001.00269.x
Rutschmann S., Matschiner M., Damerau M., Muschick M., Lehmann M.F., Hanel R. & Salzburger W. (2011). Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Molecular Ecology 20: 4707–4721. https://doi.org/10.1111/j.1365-294X.2011.05279.x
Santos-Santos J.H., Audenaert L., Verheyen E. & Adriaens D. (2015). Divergent ontogenies of trophic morphology in two closely related haplochromine cichlids. Journal of Morphology 276: 860– 871. https://doi.org/10.1002/jmor.20385
Sidlauskas B. (2008). Continuous and arrested morphological diversification in sister clades of Characiform fishes: a phylomorphospace approach. Evolution 62: 3135–3156. https://doi.org/10.1111/j.1558-5646.2008.00519.x
Stayton C.T. (2006). Testing hypotheses of convergence with multivariate data: Morphological and functional convergence among herbivorous lizards. Evolution 60: 824–841. https://doi.org/10.1111/j.0014-3820.2006.tb01160.x
Tank D.C., Eastman J.M., Pennell M.W., Soltis P.S., Soltis D.E., Hinchliff C.E., Brown J.W., Sessa E.B. & Harmon L.J. (2015). Nested radiations and the pulse of angiosperm diversification: Increased diversification rates often follow whole genome duplications. New Phytologist 207: 454–467. https://doi.org/10.1111/nph.13491
Tavera J., Acero P.A. & Wainwright P.C. (2018). Multilocus phylogeny, divergence times, and a major role for the benthic-to-pelagic axis in the diversification of grunts (Haemulidae). Molecular Phylogenetics and Evolution 121: 212–223. https://doi.org/10.1016/j.ympev.2017.12.032
Van de Putte A.P., Janko K., Kasparova E., Maes G.E., Rock J., Koubbi P., Volckaert F.A.M., Choleva L., Fraser K.P.P., Smykla J., van Houdt J.K.J. & Marshall C. (2012). Comparative phylogeography of three trematomid fishes reveals contrasting genetic structure patterns in benthic and pelagic species. Marine Genomics 8: 23–34. https://doi.org/10.1016/j.margen.2012.05.002
Wainwright P.C. & Richard B.A. (1995). Predicting patterns of prey use from morphology of fishes. Environmental Biology of Fishes 44: 97–113. https://doi.org/10.1007/BF00005909
Wainwright P.C., Bellwood D.R. & Westneat M.W. (2002). Ecomorphology of locomotion in labrid fishes. Environmental Biology of Fishes 65: 47–62. https://doi.org/10.1023/A:1019671131001
Wilson L.A.B., Colombo M., Hanel R., Salzburger W. & Sánchez-Villagra M.R. (2013). Ecomorphological disparity in an adaptive radiation: Opercular bone shape and stable isotopes in Antarctic icefishes. Ecology and Evolution 3: 3166–3182. https://doi.org/10.1002/ece3.708
Zelditch M.L., Swiderski D.L., Sheets H.D. & Fink W.L. (2004). Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, San Diego. https://doi.org/10.1016/B978-0-12-778460-1.X5000-5
