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<Italic>Kuhlia</Italic> Species The University of Chicago Evolution of Diadromy in Fish: Insights from a Tropical Genus ( Kuhlia Species). Author(s): Pierre Feutry, Magalie Castelin, Jennifer R. Ovenden, Agnès Dettaï, Tony Robinet, Corinne Cruaud, and Philippe Keith Reviewed work(s): Source: The American Naturalist, Vol. 181, No. 1 (January 2013), pp. 52-63 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/668593 . Accessed: 13/12/2012 07:34 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded on Thu, 13 Dec 2012 07:34:01 AM All use subject to JSTOR Terms and Conditions vol. 181, no. 1 the american naturalist january 2013 Evolution of Diadromy in Fish: Insights from a Tropical Genus (Kuhlia Species) Pierre Feutry,1,* Magalie Castelin,1 Jennifer R. Ovenden,2 Agne`s Dettaı¨,3 Tony Robinet,4 Corinne Cruaud,5 and Philippe Keith1 1. Muse´um National d’Histoire Naturelle, Milieux et Peuplements Aquatiques, Unite´ de Mixte de Recherche (UMR) 7208, Ichtyologie, 57 rue Cuvier, CP026, Paris 75231, France; 2. Molecular Fisheries Laboratory, Queensland Government, Ritchie Building, University of Queensland, St. Lucia, Queensland 4069, Australia; 3. Muse´um National d’Histoire Naturelle, Syste´matique et Evolution, UMR 7138, Service de Syste´matique Mole´culaire, 57 rue Cuvier, CP026, Paris 75231, France; 4. Muse´um National d’Histoire Naturelle, Milieux et Peuplements Aquatiques, UMR 7208, Station de Biologie Marine de Concarneau, Place de la Croix, 29100 Concarneau, France; 5. Genoscope, Centre National de Se´quenc¸age, 2 rue Gaston Cre´mieux, CP5706, 91057 Evry Cedex, France Submitted December 12, 2011; Accepted July 26, 2012; Electronically published November 27, 2012 Online enhancement: appendixes. the sea (Myers 1949). Diadromy takes three distinct forms: abstract: Diadromous species undergo regular migration between catadromy, anadromy, and amphidromy. Catadromous fresh and marine waters. This behavior is found in many species, including fish, mollusks, and crustaceans, some of which are com- and anadromous fish migrate between the marine and the mercially valuable species. Several attempts to trace the evolution of freshwater biomes to reproduce. Catadromous fish move this behavior have been made in Salmonidae and Galaxiidae, but from freshwater to breed in the sea, whereas anadromous ambiguous phylogenies and multiple character state changes pre- fish move from the sea to breed in freshwater habitats. vented unequivocal conclusions. The Kuhliidae family consists of 12 Migrations of amphidromous fish are not for reproductive fish species that inhabit tropical islands in the Indo-Pacific region. purposes. As defined by McDowall (2007), amphidromous The species have marine, partially catadromous, or fully catadromous life histories (i.e., they migrate from rivers to the sea to reproduce). fish reproduce in freshwater, and larvae drift downstream The evolution of migratory behavior was traced on a well-resolved to feed at sea. After a variable amount of time, juveniles phylogeny. Catadromous Kuhlia species were basal, and partially ca- return to freshwater, where they undergo most of their tadromous and marine species formed derived monophyletic groups. somatic growth before maturing and spawning. We refer This is, to our knowledge, the first time that a clear origin and polarity to this life cycle as freshwater amphidromy to distinguish for the diadromous character has been demonstrated. We propose it from marine amphidromy, which refers to reproduction that the relative lack of resources in tropical, inshore, marine habitats at sea, followed by migration to freshwater after hatching and the ephemeral and isolated nature of freshwater environments of tropical islands, combined with phenotypic plasticity of migratory for a variable period, then a return to the sea for additional traits, play key roles in driving the evolution of diadromy in the growth and reproduction (Gross 1987). Kuhliidae and probably in other groups. This work is an important Despite the physiological challenges presented by this starting point to understand the role of diadromy in speciation and tactic, diadromy has evolved multiple times in aquatic taxa, adaptation in unstable habitats. including fish, mollusks, and crustaceans, which verifies its importance. However, evolutionary pathways leading Keywords: diadromy, evolution, phylogeny, ancestral character re- construction, habitat shift, catadromy, land locking. to a diadromous life cycle are unclear (McDowall 1997). Gross (1987) proposed an ecological and evolutionary model based on the principle that diadromy would evolve Introduction if the combination of reproductive success and survivor- ship of migrants would exceed that of individuals who do The term “diadromy” was introduced by Myers to describe not migrate. In his model, catadromy and anadromy, re- migrations of aquatic organisms between freshwater and spectively, are preceded by marine and freshwater am- phidromy and are intermediary evolutionary steps be- * Corresponding author. Present address: Research Institute for Environment tween exclusively marine and freshwater life cycles. and Livelihoods, Charles Darwin University, Darwin, 0909 Northern Territory, Australia; e-mail: [email protected]. Additional analysis of global patterns in aquatic produc- Am. Nat. 2013. Vol. 181, pp. 52–63. ᭧ 2012 by The University of Chicago. tivity led to the conclusion that the presence and the di- 0003-0147/2013/18101-53512$15.00. All rights reserved. rection of diadromy can largely be explained by the relative DOI: 10.1086/668593 availability of food resources in freshwater and marine This content downloaded on Thu, 13 Dec 2012 07:34:01 AM All use subject to JSTOR Terms and Conditions Evolution of Diadromy in Kuhliidae 53 Table 1: Sample, geographical location, and species name of specimens used in this study Sample Sampling location Latitude Longitude Species identification Kmar 1 Guam 13Њ2639.5N 144Њ4737.4E Kuhlia marginata Kmar 2 New Caledonia 20Њ3128.31S 164Њ4632.56E K. marginata Kmar 3 Pentecost, VA 15Њ470.9S 168Њ 952.06E K. marginata Kmar 4 Malekula, VA 16Њ 527.79S 167Њ1030.71E K. marginata Kmar 5 Efate, VA 17Њ3715.32S 168Њ2954.42E K. marginata Kmar 6 Queensland, AU 16Њ2737.1S 145Њ2122.2E K. marginata Ksal 1 Samoa 13Њ5448.3S 171Њ445.8W Kuhlia salelea Ksal 2 Samoa 13Њ5448.3S 171Њ445.8W K. salelea Kmal 1 Moorea, FP 17Њ357.3S 149Њ5024.4W Kuhlia malo Kmal2 Raiatea, FP 16Њ5237.6S 151Њ2535.0W K. malo Krup 1 Mayotte, CO 12Њ4826.4S45Њ120.5E Kuhlia rupestris Krup 2 Re´union, MA 21Њ1832.2S55Њ2434.5E K. rupestris Krup 3 New Caledonia 20Њ3128.31S 164Њ4632.56E K. rupestris Krup 4 Fraser Island, AU 25Њ 740.6S 153Њ1740.4E K. rupestris Ksau 1 Madagascar 15Њ2660.0S47Њ400.0E Kuhlia sauvagii Ksau 2 Madagascar 15Њ 846.9S49Њ5729.4E K. sauvagii Kxen 1 Hawaii 20Њ5620.0N 156Њ2033.0W Kuhlia xenura Kxen 2 Hawaii 20Њ5620.0N 156Њ2033.0W K. xenura Kmun 1 New Caledonia 20Њ5614.7S 165Њ2241.4E Kuhlia munda Kmun 2 New Caledonia 20Њ5614.7S 165Њ2241.4E K. munda Kcau 1 Re´union, MA 21Њ1832.2S55Њ2434.5E Kuhlia caudavittata Kcau 2 Re´union, MA 21Њ1832.2S55Њ2434.5E K. caudavittata Ksan 1 Moorea, FP 17Њ3442.1S 149Њ5181.1W Kuhlia sandvicensis Ksan 2 Tubuai, FP 23Њ2229.6S 149Њ291.0W K. sandvicensis Knut 1 Easter Island 27Њ 716.3S 109Њ2159.1W Kuhlia nutabunda Knut 2 Easter Island 27Њ 716.3S 109Њ2159.1W K. nutabunda Kmug 1 Re´union, MA 21Њ1832.2S55Њ2434.5E Kuhlia mugil Kmug 2 Re´union, MA 21Њ1832.2S55Њ2434.5E K. mugil Kmug 3 Clipperton 10Њ175.4N 109Њ1258.5W K. mugil Kmug 4 Clipperton 10Њ175.4N 109Њ1258.5W K. mugil Kmug 5 New Caledonia 20Њ5550.6S 165Њ1927.6E K. mugil Kmug 6 New Caledonia 20Њ5550.6S 165Њ1927.6E K. mugil Kpet 1 Clipperton 10Њ175.4N 109Њ1258.5W Kuhlia petiti Kpet 2 Clipperton 10Њ175.4N 109Њ1258.5W K. petiti Kpet 3 Marquesas, FP 9Њ5737.50S 138Њ5028.6W K. petiti Note: AU p Australia; CO p Comoros; FP p French Polynesia; MA p Mascarene; VA p Vanuatu. habitats (Gross et al. 1988). At low latitudes, freshwater The starting point to validate Gross’s (1987) model for productivity often exceeds marine water productivity. the evolution of diadromy is to determine whether diad- Gross et al. (1988) argue that this difference promotes the romous species have freshwater, marine, or diadromous occasional excursion of marine fish into freshwater hab- ancestry. This will allow the polarity of the character (i.e., itats and initiates evolution toward a fully freshwater life migratory behavior) to be inferred, which is the key to cycle through intermediate stages of marine amphidromy understanding the evolutionary scenario. One way to ad- followed by catadromy. At high latitudes, the reverse ap- dress these issues is to focus on the phylogeny of terminal plies: ocean productivity is generally higher than fresh- taxa (e.g., within family or genus) to identify changes in water productivity,
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