Distinct migratory and non-migratory ecotypes of an endemic New Zealand eleotrid (Gobiomorphus cotidianus) – implications for incipient speciation in island freshwater fish species

Abstract

BackgroundMany postglacial lakes contain fish species with distinct ecomorphs. Similar evolutionary scenarios might be acting on evolutionarily young fish communities in lakes of remote islands. One process that drives diversification in island freshwater fish species is the colonization of depauperate freshwater environments by diadromous (migratory) taxa, which secondarily lose their migratory behaviour. The loss of migration limits dispersal and gene flow between distant populations, and, therefore, is expected to facilitate local morphological and genetic differentiation. To date, most studies have focused on interspecific relationships among migratory species and their non-migratory sister taxa. We hypothesize that the loss of migration facilitates intraspecific morphological, behavioural, and genetic differentiation between migratory and non-migratory populations of facultatively diadromous taxa, and, hence, incipient speciation of island freshwater fish species.ResultsMicrochemical analyses of otolith isotopes (88Sr, 137Ba and 43Ca) differentiated migratory and non-migratory stocks of the New Zealand endemic Gobiomorphus cotidianus McDowall (Eleotridae). Samples were taken from two rivers, one lake and two geographically-separated outgroup locations. Meristic analyses of oculoscapular lateral line canals documented a gradual reduction of these structures in the non-migratory populations. Amplified fragment length polymorphism (AFLP) fingerprints revealed considerable genetic isolation between migratory and non-migratory populations. Temporal differences in reproductive timing (migratory = winter spawners, non-migratory = summer spawners; as inferred from gonadosomatic indices) provide a prezygotic reproductive isolation mechanism between the two ecotypes.ConclusionThis study provides a holistic look at the role of diadromy in incipient speciation of island freshwater fish species. All four analytical approaches (otolith microchemistry, morphology, spawning timing, population genetics) yield congruent results, and provide clear and independent evidence for the existence of distinct migratory and non-migratory ecotypes within a river in a geographically confined range. The morphological changes within the non-migratory populations parallel interspecific patterns observed in all non-migratory New Zealand endemic Gobiomorphus species and other derived gobiid taxa, a pattern suggesting parallel evolution. This study indicates, for the first time, that distinct ecotypes of island freshwater fish species may be formed as a consequence of loss of migration and subsequent diversification. Therefore, if reproductive isolation persists, these processes may provide a mechanism to facilitate speciation.

Life-history characteristics of eleotrid fishes of the western hemisphere, and perils of life in a vanishing environment

“…The stem diadromous species in this radiation was found to be G. brevipinnis (Waters and Wallis 2001). Other studies of amphidromous species showing non-migratory (freshwater) as well as diadromous populations include the eleotrid Gobiomorphus cotidianus (Closs et al 2003;Michel et al 2008). Such variations in life history patterns are apparently also the case among the various species of Rhinogobius (Tsunagawa and Arai 2008).…”

“…Some diadromous fishes appear to follow more than a single life-history pattern among populations (facultative rather than obligate diadromy), (e.g., McDowall 1972;Waters and Wallis 2001;McDowall 2001McDowall , 2002Closs et al 2003;Iguchi 2007;Michel et al 2008). There are several studies illustrating that Gobiomorus dormitor shows such flexibility.…”

Climate change and conservation of endemic amphidromous fishes in Hawaiian streams

“…Completion of the amphi dromous life cycle requires migration from freshwater to the marine environment and back again; therefore, 'o'opu and other amphidromous fishes rely on surface water connectivity to move between spawning habitats in streams and larval habitats in the ocean. The marine larval period, which is obligate for most amphidromous species -the exception being some eleotrids (McKaye et al 1979, Erdman et al 1984, Michel et al 2008) -highlights the importance of a 'ridge-to-reef corridor' for species survival (Fitzsimons et al 1997, McDowall 1997, Radtke et al 2001, Keith 2003. Reduced or disrupted surface flow of streams and rivers represents one of the greatest threats to 'o'opu population viability (Holmquist et al 1998).…”

Genetic variation of coreoleuciscus splendidus populations (Teleostei; Cypriniformes) from four major river drainage systems in South Korea as assessed by AFLP markers

“…Amplified fragment length polymorphism (AFLP) fingerprinting technique (Vos et al, 1995;Blears et al, 1998) is a powerful tool that could provide a comprehensive picture of genetic population structuring with high resolution and reproducibility. This technique has been proven useful for genotyping or resolving genetic relationships among fish species and populations (Mickett et al, 2003;Chen et al, 2005;Ma et al, 2006;Takahashi et al, 2007;Gwo et al, 2008;Herder et al, 2008;Michel et al, 2008) and for genetic linkage mapping (Coimbra et al, 2003;McClelland and Naish, 2008). Furthermore, such information has strong implications for both the brood stock management of commercially important fisheries (Mickett et al, 2003) and the design of appropriate conservation plans for rapidly declining fish populations (Chen et al, 2005;Ma et al, 2006).…”