Abstract
Molecular genetic data suggest that June sucker (Chasmistes liorus) is only shallowly diverged from the co-occurring but phenotypically distinct Utah sucker (Catostomus ardens) in Utah Lake. Phenotypes representing both extreme morphologies (June sucker and Utah sucker) are observed in the small wild population, but relatively large numbers of intermediate phenotypes are also present. This relatively continuous variation between the two putative species could result from extensive hybridization (including reticulate evolutionary patterns) of genetically based phenotypes or incomplete divergence among lineages and extensive phenotypic plasticity with little genetic basis. To help inform the evolutionary history of June sucker and to provide critical information for management and restoration of June sucker populations, we evaluated the distribution of shape phenotypes among purebreds of each species and their hybrids and determined the heritability of shape and ecological performance between June sucker (C. liorus) and its sister species Utah sucker (C. ardens). Mouth shape of purebred June sucker and Utah sucker are located at the extremes, and hybrids are located midway between the purebreds. Multivariate heritability was relatively high for mouth shape at 0.27. Heritability for growth rate was high at 0.32–0.42, but variation was not associated with cross type. Genetically based variation in mouth shape has evolved fairly rapidly or has been maintained in the face of ongoing hybridization between the two species. Currently, there seems to be little evidence for differential selection between species that would maintain shape variation.
Similar content being viewed by others
References
Anderson TW (2003) An introduction to multivariate statistical analysis, 3rd edn. Wiley, N.J.
Araújo MS, Perez SI, Magazoni MJC, Petry AC (2014) Body size and allometric shape variation in the molly Poecilia vivipara along a gradient of salinity and predation. BMC Evol Biol 14:251
Avise JC, Walker D (2000) Abandon all species concepts? A response. Cons Genetics 1:77–80
Barluenga M, Stölting W, Salzburger MM, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719–723
Belk MC, Tuckfield RC (2011) Effect of density on growth and survival of young June sucker. Western North American Naturalist 71:490–498
Billman EJ (2008) Observations of shoaling and feeding behavior of June sucker, Chasmistes liorus, in a refuge population. Western North American Naturalist 68:390–395
Clabaut C, Bunje PME, Salzburger W, Meyer A (2007) Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution 61:560–578
Cole DD, Mock KE, Cardall BL, Crowl TA (2008) Morphological and genetic structuring in the Utah Lake sucker complex. Mol Ecol 17:5189–5204
Cooke SJ, Bunt CM, Hamilton SJ, Jennings CA, Pearson MP, Cooperman MS, Markle DF (2005) Threats, conservation strategies, and prognosis for suckers (Catostomidae) in North America: insights from regional case studies of a diverse family of non-game fishes. Biol Conserv 121:317–331
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Danley PD, Markert JA, Arnegard ME, Kocher TD (2000) Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution 54:1725–1737
Dynes J, Magnan P, Bernatchez L, Rodriguez MA (1999) Genetic and morphological variation between two forms of lacustrine brook charr. J Fish Biol 54:955–972
Eiriksson GM (1999) Heterochrony in skeletal development and body size in progeny of two morphs of Arctic charr from Thingvallavatn, Iceland. J Fish Biol 55:175–185
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman Group Ltd., Essex
Franchini P, Fruciano C, Spreitzer ML, Jones JC, Elmer KR, Henning F, Meyer A (2014) Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes. Mol Ecol 23:1828–1845. doi:10.1111/mec.12590
Fruciano C, Tigano C, Ferrito V (2012) Body shape variation and colour change during growth in a protogynous fish. Environ Biol Fish 94:615–622. doi:10.1007/s10641-011-9968-y
Hassell EMA, Meyers PJ, Billman EJ, Rasmussen JE, Belk MC (2012) Ontogeny and sex alter the effect of predation on body shape in a livebearing fish: sexual dimorphism, parallelism, and costs of reproduction. Ecology and Evolution 2:1738–1746
Hendry AP, Vamosi SM, Latham SJ, Heilbuth JC, Day T (2000) Questioning species realities. Cons Genetics 1:67–76
Howard DJ, Berlocher SH (1998) Endless forms: species and speciation. Oxford University Press, Oxford
Hulsey CD, Roberts RJ, Loh YHE, Rupp MF, Streelman JT (2013) Lake Malawi cichlid evolution along a benthic/limnetic axis. Ecology and Evolution 7:2262–2272
Ingley SJ, Billman EJ, Belk MC, Johnson JB (2014) Morphological divergence driven by predation environment within and between species of Brachyrhaphis fishes. PLoS One 9(2):e90274. doi:10.1371/journal.pone.0090274
Klingenberg CP (2003) Quantitative genetics of geometric shape: heritability and the pitfalls of the univariate approach. Evolution 57:191–195
Klingenberg CP, Leamy LJ (2001) Quantitative genetics of geometric shape in the mouse mandible. Evolution 55:2342–2352
Kristjansson BK, Skulason S, Noakes DLG (2002) Rapid divergence in a recently isolated population of threespine stickleback (Gasterosteus aculeatus L.). Evol Ecol Res 4:659–672
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ (2004) Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58:2305–2318
Manly BFJ (2006) Randomization, bootstrap and Monte Carlo methods in biology. Vol 70 (3rd edn.). CRC Press, Boca Raton
Mardia KV, Bookstein FL, Moreton IJ (2000) Statistical assessment of bilateral symmetry of shapes. Biometrika 87:285–300
Mattingly BW, Jayne BC (2004) Resource use in arboreal habitats: structure affects locomotion of four ecomorphs of Anolis lizards. Ecology 85:111–1124
Mattson E, Belk MC (2013) Intraspecific morphological variation in two common marine fish species from South Africa. Open Fish Sci J 6:87–91
Miller RR, Smith GR (1981) Distribution and evolution of Chasmistes (Pisces: Catastomidae) in western North America. Occas Pap Mus Zool Univ Mich 696:1–46
Monteiro LR, Diniz-Filho JAF, dos Reis SF, Araujo ED (2002) Geometric estimates of the heritability in biological shape. Evolution 56:563–572
Myers EM, Janzen FJ, Adams DC, Tucker JK (2006) Quantitative genetics of plastron shape in slider turtles (Trachemy scripta). Evolution 60:563–572
Naesje TF, Sandlund OT, Saksgard R (1998) Selective predation of piscivorous brown trout (Salmo trutta L.) on polymorphic whitefish (Coregonus lavaretus L.). Adv Limnol 50:283
Ostbye K, Naesje TF, Bernatchez L, Sandlund OT, Hindar K (2005) Morphological divergence and origin of sympatric populations of European whitefish (Coregonus lavaretus L.) in Lake Femund, Norway. J Evol Biol 18:683–702
Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Frontiers in Zoology 7:16. doi:10.1186/1742-9994-7-16
Pante E, Schoelinck C, Puillandre N (2015) From integrative taxonomy to species description: one step beyond. Syst Biol 64:152–160
Rader RB, Belk MC, Shiozawa DK, Crandall KA (2005) Empirical test for ecological exchangeability. Anim Conserv 8:239–247
Rencher AC (1995) Methods of multivariate analysis. Wiley, New York
Reznick DN, Shaw FH, Rodd FH, Shaw RG (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–1937
Rodríguez-Mendoza R, Muñoz M, Saborido-Rey F (2011) Ontogenetic allometry of the bluemouth, Helicolenus dactylopterus dactylopterus (Teleostei: Scorpaenidae), in the Northeast Atlantic and Mediterranean based on geometric morphometrics. Hydrobiologia 670:5–22. doi:10.1007/s10750-011-0675-7
Rogers SM, Mee JA, Bowles E (2013) The consequences of genomic architecture on ecological speciation in postglacial fishes. Current Zoology 59:53–71
Rohlf FJ, Slice D (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59
Rojas M (1992) The species problem and conservation: what are we protecting? Cons Biol 6:170–178
Schluter D (1993) Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74:699–709
Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85–108
Scoppettone GG, Vinyard G (1991) Life history and management of four endangered lacustrine suckers. In: Minckley WL Deacon JE (ed) Battle against extinction: native fish management in the American West; Symposium, Furnace Creek, California, USA, November 17–18, 1988. University of Arizona Press, Tucson, pp 359–377
Sites JW Jr, Marshall JC (2003) Delimiting species: a Renaissance issue in systematic biology. Trends Ecol Evol 18:462–470
Turgeon J, Bernatchez L (2003) Reticulate evolution and phenotypic diversity in North American ciscoes, Coregonus ssp. (Teleostei: Salmonidae): implications for the conservation of an evolutionary legacy. Conserv Genet 4:67–81
Wainwright PC (1991) Ecomorphology: experimental functional anatomy for ecological problems. Am Zool 31:680–693
Waldmann P, Ericsson T (2006) Comparison of REML and Gibbs sampling estimates of multi-trait genetic parameters in Scots pine. Theor Appl Genet 112:1441–1451
Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120
Wesner JS, Billman EJ, Meier A, Belk MC (2011) Morphological convergence during pregnancy among predator and nonpredator populations of the livebearing fish Brachyrhaphis rhabdophora (Teleostei: Poeciliidae). Biol J Linn Soc 104:386–392
Whitney M, Belk MC (2000) Threatened fishes of the world: Chasmistes liorus Jordan, 1878 (Catostomidae). Environ Biol Fish 57:362
Wund MA, Valena S, Wood S, Baker JA (2012) Ancestral plasticity and allometry in threespine stickleback reveal phenotypes associated with derived, freshwater ecotypes. Biol J Linn Soc 105(3):573–583. doi:10.1111/j.1095-8312.2011.01815.x
Acknowledgments
We thank Eric Harvey, Josh Rasmussen, Doug Routledge, Eriek Hansen, Krissy Wilson, Mike Mills, Clay Peck, and numerous BYU undergraduate students who worked on all phases of the research. Funding was provided by the June Sucker Recovery Program through the Utah Division of Wildlife Resources. All experiments were approved through the Institutional Animal Care and Use Committee at Brigham Young University.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Nico Posnien and Nikola-Michael Prpic
This article is part of the Special Issue “Size and Shape: Integration of morphometrics, mathematical modelling, developmental and evolutionary biology”, Guest Editors: Nico Posnien—Nikola-Michael Prpic.
Rights and permissions
About this article
Cite this article
Belk, M.C., Schaalje, G.B. Multivariate heritability of shape in June sucker (Chasmistes liorus) and Utah sucker (Catostomus ardens): shape as a functional trait for discriminating closely related species. Dev Genes Evol 226, 197–207 (2016). https://doi.org/10.1007/s00427-016-0547-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-016-0547-2