Evolution of diadromy in fish: insights from a tropical genus (Kuhlia species)

Diadromous species undergo regular migration between fresh and marine waters. This behavior is found in many species, including fish, mollusks, and crustaceans, some of which are commercially valuable species. Several attempts to trace the evolution of this behavior have been made in Salmonidae and Galaxiidae, but ambiguous phylogenies and multiple character state changes prevented unequivocal conclusions. The Kuhliidae family consists of 12 fish species that inhabit tropical islands in the Indo-Pacific region. The species have marine, partially catadromous, or fully catadromous life histories (i.e., they migrate from rivers to the sea to reproduce). The evolution of migratory behavior was traced on a well-resolved phylogeny. Catadromous Kuhlia species were basal, and partially catadromous and marine species formed derived monophyletic groups. This is, to our knowledge, the first time that a clear origin and polarity for the diadromous character has been demonstrated. We propose that the relative lack of resources in tropical, inshore, marine habitats and the ephemeral and isolated nature of freshwater environments of tropical islands, combined with phenotypic plasticity of migratory traits, play key roles in driving the evolution of diadromy in the Kuhliidae and probably in other groups. This work is an important starting point to understand the role of diadromy in speciation and adaptation in unstable habitats

Contrasting Genetic Structure among Populations of Two Amphidromous Fish Species (Sicydiinae) in the Central West Pacific

Both present-day and past processes can shape connectivity of populations. Pleistocene vicariant events and dispersal have shaped the present distribution and connectivity patterns of aquatic species in the Indo-Pacific region. In particular, the processes that have shaped distribution of amphidromous goby species still remain unknown. Previous studies show that phylogeographic breaks are observed between populations in the Indian and Pacific Oceans where the shallow Sunda shelf constituted a geographical barrier to dispersal, or that the large spans of open ocean that isolate the Hawaiian or Polynesian Islands are also barriers for amphidromous species even though they have great dispersal capacity. Here we assess past and present genetic structure of populations of two amphidromous fish (gobies of the Sicydiinae) that are widely distributed in the Central West Pacific and which have similar pelagic larval durations. We analysed sections of mitochondrial COI, Cytb and nuclear Rhodospine genes in individuals sampled from different locations across their entire known range. Similar to other Sicydiinae fish, intraspecific mtDNA genetic diversity was high for all species (haplotype diversity between 0.9-0.96). Spatial analyses of genetic variation in Sicyopus zosterophorum demonstrated strong isolation across the Torres Strait, which was a geologically intermittent land barrier linking Australia to Papua New Guinea. There was a clear genetic break between the northwestern and the southwestern clusters in Si. zosterophorum (phi(ST) = 0.67502 for COI) and coalescent analyses revealed that the two populations split at 306 Kyr BP (95% HPD 79-625 Kyr BP), which is consistent with a Pleistocene separation caused by the Torres Strait barrier. However, this geographical barrier did not seem to affect Sm. fehlmanni. Historical and demographic hypotheses are raised to explain the different patterns of population structure and distribution between these species. Strategies aiming to conserve amphidromous fish should consider the presence of cryptic evolutionary lineages to prevent stock depletion

Pelagic larval duration of two diadromous species of Kuhliidae (Teleostei: Percoidei) from Indo-Pacific insular systems

Diadromous fish species in the family Kuhliidae are able to colonise freshwater systems in Indo-Pacific islands, but their life cycle and the mechanisms involved in the colonisation of such ecosystems are poorly documented. After validating the daily rate of increment deposition in otoliths of Kuhlia rupestris, we estimated the pelagic larval duration (PLD) of K. rupestris, widely distributed in the Indo-Pacific area, and K. sauvagii, endemic to the Indian Ocean. Median PLD of K. rupestris was significantly longer than that of K. sauvagii (40.6±6.9 and 32.3±3.4 days ( s.d.), respectively), implying that the PLD is probably one factor controlling the extent of distribution range in Kuhlia. Within K. rupestris, individuals from New Caledonia had longer PLDs than those from Ŕunion Island (44.3±6.7 and 37.3±4.7 days (±s.d.) respectively). Further research on larval migration is needed to determine whether this was due to different environmental conditions or is population-specific. Interestingly, the PLD of these Kuhlia species is shorter than the PLD of other tropical diadromous fishes. These results improve our understanding of the dispersal strategies of freshwater fauna, to colonise and persist in tropical islands

Data from: Stretched to the limit; can a short pelagic larval duration connect adult populations of an Indo-Pacific diadromous fish (Kuhlia rupestris)?

Freshwater species on tropical islands face localized extinction and the loss of genetic diversity. Their habitats can be ephemeral due to variability in freshwater run-off and erosion. Even worse, anthropogenic effects on these ecosystems are intense. Most of these species are amphidromous or catadromous (i.e. their life cycle includes a marine larval phase), which buffers them against many of these effects. A long pelagic larval duration (PLD) was thought to be critical to ensure the colonization and persistence in tropical islands, but recent findings indicated that several species with short PLDs are successful in those ecosystems. To test the potential of a short PLD in maintaining genetic connectivity and forestalling extirpation, we studied Kuhlia rupestris, a catadromous fish species with an extensive distribution in the western Pacific and Indian Oceans. Using a combination of molecular genetic markers (13 microsatellite loci and two gene regions from mtDNA) and modelling of larval dispersal, we show that a short PLD constrains genetic connectivity over a wide geographical range. Molecular markers showed that the short PLD did not prevent genetic divergence through evolutionary time and speciation has occurred or is occurring. Modelling of larvae dispersal suggested limited recent connectivity between genetically homogeneous populations across the Coral Sea. However, a short PLD can maintain connectivity on a subocean basin scale. Conservation and management of tropical diadromous species needs to take into account that population connectivity may be more limited than previously suspected in those species

Stretched to the limit; can a short pelagic larval duration connect adult populations of an Indo-Pacific diadromous fish (Kuhlia rupestris)?

Freshwater species on tropical islands face localized extinction and the loss of genetic diversity. Their habitats can be ephemeral due to variability in freshwater run-off and erosion. Even worse, anthropogenic effects on these ecosystems are intense. Most of these species are amphidromous or catadromous (i.e. their life cycle includes a marine larval phase), which buffers them against many of these effects. A long pelagic larval duration (PLD) was thought to be critical to ensure the colonization and persistence in tropical islands, but recent findings indicated that several species with short PLDs are successful in those ecosystems. To test the potential of a short PLD in maintaining genetic connectivity and forestalling extirpation, we studied Kuhlia rupestris, a catadromous fish species with an extensive distribution in the western Pacific and Indian Oceans. Using a combination of molecular genetic markers (13 microsatellite loci and two gene regions from mtDNA) and modelling of larval dispersal, we show that a short PLD constrains genetic connectivity over a wide geographical range. Molecular markers showed that the short PLD did not prevent genetic divergence through evolutionary time and speciation has occurred or is occurring. Modelling of larvae dispersal suggested limited recent connectivity between genetically homogeneous populations across the Coral Sea. However, a short PLD can maintain connectivity on a subocean basin scale. Conservation and management of tropical diadromous species needs to take into account that population connectivity may be more limited than previously suspected in those species

Phylogenetic relationship between <i>Sicyopus zosterophorum</i>, <i>Smilosicyopus fehlmanni</i> and <i>Smilosicyopus chloe</i>.

<p>The rooted phylogram was drawn using 760-joining methods using Kimura two-parameter distances (K2P). NW and SW refers to northwest and southwest biogeographic regions within <i>Si. Zosterophorum</i> samples.</p

Pairwise F-statistics for 3 populations of <i>Smilosicyopus fehlmanni</i>.

<p>Pairwise φ_ST for COI data are below diagonal and p-values are above diagonal. Only populations with more than 5 individuals were taken into account. Populations are labeled according to <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0075465#pone-0075465-t001" target="_blank">Table 1</a> (country).</p

Pairwise F-statistics for 6 populations of <i>Sicyopus zosterophorum</i>.

<p>Pairwise φ_ST for COI data are below diagonal and p-values are above diagonal. Only populations with more than 5 individuals were taken into account. Populations are labeled according to <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0075465#pone-0075465-t001" target="_blank">Table 1</a> (country).</p

Hierarchical partitioning of molecular variation (AMOVA) based on COI haplotypes within and among southwest and northwest Pacific groups and populations for <i>Si. zosterophorum</i>.

<p>Hierarchical partitioning of molecular variation (AMOVA) based on COI haplotypes within and among southwest and northwest Pacific groups and populations for <i>Si. zosterophorum</i>.</p