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Contrasting Evolutionary Pathways of Anadromy in Euteleostean Fishes

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Contrasting Evolutionary Pathways of Anadromy in Euteleostean Fishes American Fisheries Society Symposium 69:63–77, 2009 © 2009 by the American Fisheries Society Contrasting Evolutionary Pathways of Anadromy in Euteleostean Fishes JULIAN J. DO D SON * Département de biologie, Université Laval, Pavillon Vachon, Québec G1V 0A6, Canada JÉRÔME LAROCHE Centre de bioinformatique et de biologie computationnelle, Université Laval Pavillon Marchand, Québec G1V 0A6, Canada FRÉ D ÉRIC LECOMTE 1 Département de biologie, Université Laval, Pavillon Vachon, Québec G1V 0A6, Canada Abstract.—We develop the view, based on life cycle differences and recently published sister group relationships, that the freshwater life cycle was the ancestral character state lead- ing to anadromy among salmoniforms, whereas the marine life cycle was the ancestral char- acter state leading to anadromy among osmeriforms. In contrast to most salmonid fishes, the reproductive migrations of smelts are generally characterized by brief excursions to spawn in freshwater, and larvae may spend no more than 24 h in freshwater before being transported to coastal marine or estuarine environments. We reconstructed the phylogeny of the sub- order Osmeroidei to establish the phylogenetic relationships among anadromous, marine, and freshwater species of this taxon. We mapped these life cycles onto phylogenetic trees of osmeriforms and salmoniforms and applied character-reconstruction methodology based on simple parsimony and likelihood methodologies. A freshwater origin of salmonids was supported by our analyses, whereas either marine or anadromous life cycles characterized the evolution of osmeroids. The possibility that the evolution of anadromy in salmonids and osmeroids followed separate paths requires a reconsideration of some generalizations concerning anadromy. We hypothesize that anadromy in osmeroids may be first and fore- most an adaptation to place embryos and the early larval stages in reproductive safe sites to maximize their survival. The evolution of exclusive freshwater species of osmeriforms has oc- curred via anadromy through the various processes associated with landlocking. Freshwater amphidromy in osmeroids is most likely a consequence of anadromy rather than a precursor and may be contingent upon the availability of food resources in freshwater. Finally, marine osmeroids have been derived from anadromous ancestors and are “safe-site” specialists, ex- ploiting principally the upper intertidal zone for reproduction. We also suggest that such contrasting evolutionary pathways to anadromy may provide insight into the evolution of partial migration, observed uniquely in salmonids, and the nature and extent of population genetic structure found in the two groups of fishes. Introduction feeding (diadromy) exhibit three migratory pat- terns (Myers 1949). Anadromous fishes such as Fishes that migrate regularly between freshwater salmon move from the sea to breed in freshwater, and saltwater for the purposes of reproduction and whereas catadromous fishes such as eels move from freshwater to breed in the sea. The third category, * Corresponding author: julian.dodson@bio.ulaval.ca 1 Current address: INRA, UMR ECOBIOP, Quartier Ibarron, amphidromy, is sometimes included within either 64310 St Pée-sur-Nivelle, France anadromy or catadromy but has been considered 63 64 dodson et al. as a distinct strategy (McDowall 1988). McDowall and the ultimate derived state involves a complete- (2004) restricted the definition of amphidromy to ly marine life cycle. fishes that reproduce in freshwater and drift down- Since they were first published, these com- stream following hatching to feed at sea for vari- prehensive evolutionary scenarios have generated able periods of time before returning to freshwater a great deal of discussion and ensuing confusion. to feed and grow to maturity. We refer to this life McDowall (1997) objected to the contention that cycle more specifically as freshwater amphidromy amphidromy is an intermediate stage in the evolu- to distinguish it from those diadromous fishes that tion of anadromy on the basis that there are few reproduce at sea, migrate to freshwater early in life documented cases of freshwater fishes becoming to feed for variable periods of time, and return to sea facultative marine wanderers, the initial stage in to feed and grow to maturity (marine amphidromy, Gross’ evolutionary pathway to anadromy. How- Gross 1987). Diadromy is shown by at least 227 fish ever, McDowall (1988) defined a category of fresh- species, of which 110 are anadromous (McDowall water fishes that occasionally move into marine wa- 1988; Nelson 1994). Anadromy appears to have ters (euryhaline wanderers) as being distinct from evolved early among fishes, as 90% of the 110 spe- anadromous fishes. The well-documented ability of cies identified by McDowall (1988) as anadromous many freshwater species to exploit the oligohaline are among either the most primitive living fishes waters of estuaries (Moyle and Cech 2004) seems to (e.g., lampreys, sturgeons; 20 species) or the basal fit the definition of euryhaline wanderers and rep- clupeocephalan teleosts (79 species.). However, its resents a plausible evolutionary route to an anadro- presence among some neoteleosts (e.g., Gasterostei- mous life style. McDowall (1997) also stated that formes, Gobioidei) suggests more than one inde- there is little empirical evidence that marine amphi- pendent origin of anadromy. dromy is a precursor to the evolution of catadromy One of the most influential contributions to in formerly marine species as there are virtually no understanding the adaptive significance and evolu- cases of amphidromous species that spawn at sea. tion of diadromy was formulated by Gross (1987). On the contrary, recent observations reveal that ma- To evolve, diadromy (or any other migratory pat- rine amphidromy is more common than previously tern) must result in a level of lifetime reproduc- suggested, even among the catadromous anguillid tive success (reproductive success 3 survivorship) eels (Daverat et al. 2006 and references therein). exceeding that of individuals who do not migrate. Despite numerous publications on the subject, we The most important biological variable in explain- are no closer to formulating a comprehensive evolu- ing the presence and direction of diadromy was tionary framework to understand the development identified as the relative availability of food in ma- of diadromy beyond that provided by Gross (1987) rine and freshwater habitats (Gross et al. 1988). 20 years ago. In the present paper, we aim to pro- Marine habitats are more productive at high lati- vide an alternative, yet complementary, model of tudes and less so towards the tropics, whereas the the evolution of anadromy. inverse occurs in freshwater. As such, anadromy The starting point of this argument is to chal- is favored at high latitudes, whereas catadromy is lenge the assumption that anadromy has been favored at low latitudes. Gross (1987) envisioned uniquely derived from freshwater origins. Several amphidromy as the ancestral state in the evolution anadromous fishes such as the Atlantic tomcod Mi- of anadromy and catadromy. Finally, the evolu- crogadus tomcod (Walbaum) and the clupeid shads tionary scenarios proposed by Gross (1987) were (Alosa spp. and Hilsa spp.) appear to have been based on the assumption that the ancestral state of derived from marine families (McDowall 1993, diadromous fishes involves the reproductive envi- 1997; Dodson 1997). Secor (2002) hypothesized ronment. As such, catadromous fishes are derived that anadromy in striped bass Morone saxatilis from marine species that continue to exploit the (Walbaum) evolved from a marine-spawning ances- ancestral reproductive environment. The ultimate tor. Gobies may represent another, more complex, derived state involves a completely freshwater life example. The suborder Gobioidei is sister to the cycle. On the other hand, anadromous fishes are widespread, primarily marine family Apogonidae. derived from freshwater species that continue to The phylogenetic analysis of Thacker and Hardman exploit the ancestral reproductive environment (2005) supports the hypothesis that gobioids arose evolution of anadromy in euteleostean fishes 65 in freshwater, from a marine ancestor, then returned son 1994), and the suborder Osmeroidei (the dia- to marine habitats on several occasions. Of the 42 dromous smelts, galaxiids, and icefishes) are the two valid genera of basal gobioid families identified by major clades peripheral to the basal neoteleosts, all Thacker and Hardman (2005), 17 are classified as of which are marine species. The maximum parsi- having freshwater life cycles, 17 as salt-tolerant, oc- mony analysis of Ishiguro et al. (2003) revealed that curring in freshwater and estuaries, and 8 as having Argentoidae is the sister group to Osmeroidei, and marine life cycles. Exclusively freshwater ecology is together, they form the sister group of neoteleosts. optimized as the condition at the root of Gobioidei, It thus appears plausible that anadromy among os- and invasion of marine habitats is hypothesized to meroids may have evolved from marine origins. In have occurred independently on several occasions. contrast to salmoniforms, reproduction in freshwa- The major radiation of Gobioidei, the gobiine go- ter of anadromous osmeroids may be considered the biids, is known primarily from marine habitats. The derived state. The emergence of anadromy may thus occurrence of the anadromous life history strategy have followed very different
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