Abstract
Domestication has a dominant and increasing influence on the evolutionary trajectory of species, the extent of which may be influenced by advertent selection used to meet consumer demands of the ornamental trade. Ornamental species can have multiple varieties in trade, including those produced without advertent selection for color (i.e., inadvertent selection). Consumer demand for colorful varieties can have invasion consequences because demand is related to propagule pressure and color can exhibit fitness costs. However, domesticated varieties can also adapt to wild conditions through feralization, changing the phenotypes of feral populations. Our objective was to examine how domestication and feralization together influence the feral distribution and phenotypes of two highly domesticated, ornamental poeciliids. We first determined that colorful varieties exhibited higher trade availability and local production than the wild-type variety. Using a multi-year landscape-scale survey, we then determined that colorful varieties are common near sources of production but attenuated at increasing distance, replaced by the wild-type form. Wild-type varieties exhibited trait differences from ornamental varieties, which may affect fitness and result from feralization. Domestication to meet consumer demand influences feral distributions and phenotypes of escaped fish, but only in proximity to sources of production. Feralization influences relative capture rate of ornamental versus wild-type varieties, as well as the traits of captured fish. Thus, there may be a balance between propagule pressure, thought to increase with trade volume, and the pattern of domestication and feralization selection, which affects feral distribution and phenotypes.
Similar content being viewed by others
References
Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) Synthesis: fitness of hatchery-reared salmonids in the wild. Evol Appl 1:342–355. https://doi.org/10.1111/j.1752-4571.2008.00026.x
Avery M, Eiselman D, Young M et al (1999) Wading bird predation at tropical aquaculture facilities in central Florida. N Am J Aquac 61:64–69
Balon E (2004) About the oldest domesticates among fishes. J Fish Biol 65:1–27. https://doi.org/10.1111/j.1095-8649.2004.00563.x
Basolo AL, Alcaraz G (2003) The turn of the sword: length increases male swimming costs in swordtails. Proc R Soc B Biol Sci 270:1631–1636. https://doi.org/10.1098/rspb.2003.2388
Basolo AL, Wagner WE (2004) Covariation between predation risk, body size and fin elaboration in the green swordtail, Xiphophorus helleri. Biol J Linn Soc 83:87–100. https://doi.org/10.1111/j.1095-8312.2004.00369.x
Bleakley BH, Martell CM, Brodie ED (2006) Variation in anti-predator behavior among five strains of inbred guppies, Poecilia reticulata. Behav Genet 36:783–791. https://doi.org/10.1007/s10519-005-9044-5
Cameron AC, Trivedi PK (1990) Regression-based tests for overdispersion in the Poisson model. J Econom 46:347–364. https://doi.org/10.1016/0304-4076(90)90014-K
Chan FT, Beatty SJ, Gilles AS et al (2019) Leaving the fish bowl: the ornamental trade as a global vector for freshwater fish invasions. Aquat Ecosyst Heal Manag 22:417–439. https://doi.org/10.1080/14634988.2019.1685849
Christie MR, Marine ML, French RA, Blouin MS (2012) Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci 109:238–242. https://doi.org/10.1073/pnas.1111073109
Courtenay WR, Sahlman HF, Miley WW, Herrema DJ (1974) Exotic fishes in fresh and brackish waters of Florida. Biol Conserv 6:292–302. https://doi.org/10.1016/0006-3207(74)90008-1
D’Amore DM, Popescu VD, Morris MR (2019) The influence of the invasive process on behaviours in an intentionally introduced hybrid, Xiphophorus helleri–maculatus. Anim Behav 156:79–85. https://doi.org/10.1016/j.anbehav.2019.08.009
Deacon AE, Ramnarine IW, Magurran AE (2011) How reproductive ecology contributes to the spread of a globally invasive fish. PLoS ONE 6:e24416. https://doi.org/10.1371/journal.pone.0024416
Diaz Pauli B, Wiech M, Heino M, Utne-Palm AC (2015) Opposite selection on behavioural types by active and passive fishing gears in a simulated guppy Poecilia reticulata fishery. J Fish Biol 86:1030–1045. https://doi.org/10.1111/jfb.12620
Domyan ET, Shapiro MD (2017) Pigeonetics takes flight: evolution, development, and genetics of intraspecific variation. Dev Biol 427:241–250
Drake AG, Klingenberg CP (2010) Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am Nat 175:289–301. https://doi.org/10.1086/650372
Drake JM, Baggenstos P, Lodge DM (2005) Propagule pressure and persistence in experimental populations. Biol Lett 1:480–483. https://doi.org/10.1098/rsbl.2005.0375
Duarte CM, Marbá N, Holmer M (2007) Rapid domestication of marine species. Science 316:382–383. https://doi.org/10.1126/science.1138042
Duggan IC, Rixon CAM, MacIsaac HJ (2006) Popularity and propagule pressure: determinants of introduction and establishment of aquarium fish. Biol Invasions 8:377–382. https://doi.org/10.1007/s10530-004-2310-2
Eklöv P, Jonsson P (2007) Pike predators induce morphological changes in young perch and roach. J Fish Biol 70:155–164. https://doi.org/10.1111/j.1095-8649.2006.01283.x
Ellender BR, Weyl OLF (2014) A review of current knowledge, risk and ecological impacts associated with non-native freshwater fish introductions in South Africa. Aquat Invasions 9:117–132. https://doi.org/10.3391/ai.2014.9.2.01
Endler JA (1983) Natural and sexual selection on color patterns in poeciliid fishes. Environ Biol Fishes 9:173–190. https://doi.org/10.1007/BF00690861
Gering E, Incorvaia D, Henriksen R et al (2019) Getting back to nature: feralization in animals and plants. Trends Ecol Evol 34:1137–1151. https://doi.org/10.1016/j.tree.2019.07.018
Godin JGJ, McDonough HE (2003) Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav Ecol 14:194–200. https://doi.org/10.1093/beheco/14.2.194
Gordon M (1937) Heritable color variations in the Mexican swordtail-fish: aquarium species as the drosophila of fish genetics. J Hered 28:223–230. https://doi.org/10.1093/oxfordjournals.jhered.a104368
Greenfield DW, Thomerson JE (1997) Fishes of the continental waters of Belize. University Press of Florida, Gainesville
Hill JE, Tuckett QM (2018) Abiotic and biotic contributions to invasion resistance for ornamental fish in west-central Florida, USA. Hydrobiologia 817:363–377. https://doi.org/10.1007/s10750-017-3496-5
Hill JE, Yanong RPE (2016) Freshwater ornamental fish commonly cultured in Florida. University of Florida IFAS Extension, Circular, p 54
Hill JE, Kapuscinski AR, Pavlowich T (2011) Fluorescent transgenic Zebra danio more vulnerable to predators than wild-type fish. Trans Am Fish Soc 140:1001–1005. https://doi.org/10.1080/00028487.2011.603980
Howard RD, Rohrer K, Liu Y, Muir WM (2015) Mate competition and evolutionary outcomes in genetically modified zebrafish (Danio rerio). Evolution (N Y) 69:1143–1157. https://doi.org/10.1111/evo.12662
Hutchings JA (2014) Unintentional selection, unanticipated insights: introductions, stocking and the evolutionary ecology of fishes. J Fish Biol 85:1907–1926. https://doi.org/10.1111/jfb.12545
Hutchings JA, Fraser DJ (2008) The nature of fisheries-and farming-induced evolution. Mol Ecol 17:294–313. https://doi.org/10.1111/j.1365-294X.2007.03485.x
Karino K, Haijima Y (2001) Heritability of male secondary sexual traits in feral guppies in Japan. J Ethol 19:33–37. https://doi.org/10.1088/0953-2048/18/2/036
Kingston J, Rosenthal G, Ryan M (2003) The role of sexual selection in maintaining a colour polymorphism in the pygmy swordtail, Xiphophorus pygmaeus. Anim Behav 65:735–743. https://doi.org/10.1006/anbe.2003.2110
Lawson LL, Tuckett QM, Lawson KM et al (2015) Lower lethal temperature for arapaima Arapaima gigas: Potential implications for culture and establishment in Florida. N Am J Aquac 77:497–502. https://doi.org/10.1080/15222055.2015.1066471
Lawson KM, Tuckett QM, Ritch JL et al (2017) Distribution and status of five non-native fish species in the Tampa Bay drainage (USA), a hot spot for fish introductions. BioInvasions Rec 6:393–406
Leggatt RA, Dhillon RS, Mimeault C et al (2018) Low-temperature tolerances of tropical fish with potential transgenic applications in relation to winter water temperatures in Canada. Can J Zool 96:253–260. https://doi.org/10.1139/cjz-2017-0043
Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. https://doi.org/10.1016/j.tree.2005.02.004
Maceda-Veiga A, Cable J (2019) Diseased fish in the freshwater trade: from retailers to private aquarists. Dis Aquat Organ 132:157–162. https://doi.org/10.3354/dao03310
Magalhães ALB, Jacobi CM (2017) Colorful invasion in permissive Neotropical ecosystems: establishment of ornamental non-native poeciliids of the genera Poecilia/Xiphophorus (Cyprinodontiformes: Poeciliidae) and management alternatives. Neotrop Ichthyol 15:1–14. https://doi.org/10.1590/1982-0224-20160094
Magalhães ALB, Brito MFG, Sarrouh B (2019) An inconvenient routine: Introduction, establishment and spread of new non-native fishes in the paraíba do sul river basin, state of minas Gerais, Brazil. Neotrop Biol Conserv 14:329–338. https://doi.org/10.3897/neotropical.14.e38058
McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall/CRC, London
Meffin R, Duncan RP, Hulme PE (2018) Testing weed risk assessment paradigms: intraspecific differences in performance and naturalisation risk outweigh interspecific differences in alien Brassica. J Appl Ecol 55:516–525. https://doi.org/10.1111/1365-2664.12993
Ortega JCG, Júlio HF, Gomes LC, Agostinho AA (2014) Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia 746:147–158. https://doi.org/10.1007/s10750-014-2025-z
Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Environ 2:131–138. https://doi.org/10.2307/3868238
Pyke GH (2008) Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu Rev Ecol Evol Syst 39:171–191. https://doi.org/10.1146/annurev.ecolsys.39.110707.173451
Reznick D, Endler JA (1982) The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution (N Y) 36:160–177
Rixon CAM, Duggan IC, Bergeron NMN et al (2005) Invasion risks posed by the aquarium trade and live fish markets on the Laurentian Great Lakes. Biodivers Conserv 14:1365–1381. https://doi.org/10.1007/s10531-004-9663-9
Santostefano F, Fanson KV, Endler JA, Biro PA (2019) Behavioral, energetic, and color trait integration in male guppies: testing the melanocortin hypothesis. Behav Ecol 30:1539–1547. https://doi.org/10.1093/beheco/arz109
Shafland P, Gestring K, Stanford M (2008) Florida’s exotic freshwater fishes-2007. Florida Sceintist 71:220–245
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102. https://doi.org/10.1146/annurev.ecolsys.110308.120304
Smallbone W, van Oosterhout C, Cable J (2016) The effects of inbreeding on disease susceptibility: Gyrodactylus turnbulli infection of guppies, Poecilia reticulata. Exp Parasitol 167:32–37. https://doi.org/10.1016/j.exppara.2016.04.018
Strecker A, Campbell P, Olden J (2011) The aquarium trade as an invasion pathway in the Pacific Northwest. Fisheries 36:74–85
Sundström LF, Petersson E, Höjesjö J et al (2004) Hatchery selection promotes boldness in newly hatched brown trout (Salmo trutta): Implications for dominance. Behav Ecol 15:192–198. https://doi.org/10.1093/beheco/arg089
Teletchea F (2016) Is fish domestication going too fast? Nat Resour 7:399–404. https://doi.org/10.4236/nr.2016.76034
Tuckett QM, Ritch JL, Lawson KM, Hill JE (2016) Implementation and enforcement of best management practices for Florida ornamental aquaculture with an emphasis on nonnative species. N Am J Aquac 78:113–124. https://doi.org/10.1080/15222055.2015.1121176
Tuckett QM, Ritch JL, Lawson KM, Hill JE (2017) Landscape-scale survey of non-native fishes near ornamental aquaculture facilities in Florida, USA. Biol Invasions 19:223–237. https://doi.org/10.1007/s10530-016-1275-2
Vellend M, Drummond EBM, Tomimatsu H (2010) Effects of genotype identity and diversity on the invasiveness and invasibility of plant populations. Oecologia 162:371–381. https://doi.org/10.1007/s00442-009-1480-0
White S, Miller W, Dowell S et al (2018) Limited hatchery introgressions into wild brook trout (Salvelinus fontinalis) populations despite reocurring stocking. Evol Appl 11:1567–1581. https://doi.org/10.1111/eva.12646
Acknowledgements
We thank our farm cooperators and the Florida Tropical Fish Farms Association. This research would not have been possible without their support. We also thank current and former staff at the Florida Department of Agriculture and Consumer Services Division of Aquaculture, including Joe Clayton, Kal Knickerbocker, Serina Rocco, and Portia Sapp. Assistance with field sampling was provided by David Cray, Lauren Partridge, Bryanna Poli, Holly Salg, and Mitchell Stanton.
Funding
This study was supported by the University of Florida/IFAS School of Forest Resources and Conservation, Tropical Aquaculture Laboratory, and grants from the Florida Department of Agriculture and Consumer Services’ Division of Aquaculture.
Author information
Authors and Affiliations
Contributions
QMT and JEH designed the study, QMT, KNR, JLR, KML, and JEH acquired the data, QMT analyzed the data, QMT, KNR, and KML drafted the document, QMT, KNR, JLR, KML, and JEH edited the document.
Corresponding author
Ethics declarations
Human and animal rights
The authors followed all relevant institutional guidelines for the use of vertebrate animals. The research was conducted under UF IACUC #201509018.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tuckett, Q.M., Ressel, K.N., Ritch, J.L. et al. Domestication and feralization influence the distribution and phenotypes of escaped ornamental fish. Biol Invasions 23, 1033–1047 (2021). https://doi.org/10.1007/s10530-020-02415-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-020-02415-1