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Patagonia is one of the few areas in the Southern Hemisphere to have been directly influenced by Quaternary glaciers. In this study, we evaluate the influence that Quaternary glacial ice had on the genetic diversity of two congeneric fish species, the diadromous Galaxias maculatus and the nondiadromous Galaxias platei, using multilocus estimates of effective population size through time. Mid-Quaternary glaciations had far-reaching consequences for both species. Galaxias maculatus and G. platei each experienced severe genetic bottlenecks during the period when Patagonia ice sheet advance reached its maximum positions c. 1.1-0.6 Ma. Concordant drops in effective size during this time suggest that range sizes were under similar constraints. It is therefore unlikely that coastal (brackish/marine) environments served as a significant refuge for G. maculatus during glacial periods. An earlier onset of population declines for G. platei suggests that this species was vulnerable to modest glacial advances. Declines in effective sizes were continuous for both species and lasted into the late-Pleistocene. However, G. maculatus exhibited a strong population recovery during the late-Quaternary (c. 400,000 bp). Unusually long and warm interglacials associated with the late-Quaternary may have helped to facilitate a strong population rebound in this primarily coastal species.

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BACKGROUND: The dynamic geological and climatic histories of temperate South America have played important roles in shaping the contemporary distributions and genetic diversity of endemic freshwater species. We use mitochondria and nuclear sequence variation to investigate the consequences of mountain barriers and Quaternary glacial cycles for patterns of genetic diversity in the diadromous fish Galaxias maculatus in Patagonia (approximately 300 individuals from 36 locations). RESULTS: Contemporary populations of G. maculatus, east and west of the Andes in Patagonia, represent a single monophyletic lineage comprising several well supported groups. Mantel tests using control region data revealed a strong positive relationship when geographic distance was modeled according to a scenario of marine dispersal. (r = 0.69, P = 0.055). By contrast, direct distance between regions was poorly correlated with genetic distance (r = -0.05, P = 0.463). Hierarchical AMOVAs using mtDNA revealed that pooling samples according to historical (pre-LGM) oceanic drainage (Pacific vs. Atlantic) explained approximately four times more variance than pooling them into present-day drainage (15.6% vs. 3.7%). Further post-hoc AMOVA tests revealed additional genetic structure between populations east and west of the Chilean Coastal Cordillera (coastal vs. interior). Overall female effective population size appears to have remained relatively constant until roughly 0.5 Ma when population size rapidly increased several orders of magnitude [100x (60x-190x)] to reach contemporary levels. Maximum likelihood analysis of nuclear alleles revealed a poorly supported gene tree which was paraphyletic with respect to mitochondrial-defined haplogroups. CONCLUSIONS: First diversifying in the central/north-west region of Patagonia, G. maculatus extended its range into Argentina via the southern coastal regions that join the Pacific and Atlantic oceans. More recent gene flow between northern populations involved the most ancient and most derived lineages, and was likely facilitated by drainage reversal(s) during one or more cooling events of the late Pleistocene. Overall female effective population size represents the end result of a widespread and several hundred-fold increase over approximately 0.5 Ma, spanning several climatic fluctuations of the Pleistocene. The minor influence of glacial cycles on the genetic structure and diversity of G. maculatus likely reflects the access to marine refugia during repeated bouts of global cooling. Evidence of genetic structure that was detected on a finer scale between lakes/rivers is most likely the result of both biological attributes (i.e., resident non-migratory behavior and/or landlocking and natal homing in diadromous populations), and the Coastal Cordillera as a dispersal barrier.

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We employed DNA sequence variation at two mitochondrial (control region, COI) regions from 212 individuals of Galaxias platei (Pisces, Galaxiidae) collected throughout Patagonia (25 lakes/rivers) to examine how Andean orogeny and the climatic cycles throughout the Quaternary affected the genetic diversity and phylogeography of this species. Phylogenetic analyses revealed four deep genealogical lineages which likely represent the initial division of G. platei into eastern and western lineages by Andean uplift, followed by further subdivision of each lineage into separate glacial refugia by repeated Pleistocene glacial cycles. West of the Andes, refugia were likely restricted to the northern region of Patagonia with small relicts in the south, whereas eastern refugia appear to have been much larger and widespread, consisting of separate northern and southern regions that collectively spanned most of Argentinean Patagonia. The retreat of glacial ice following the last glacial maximum allowed re-colonization of central Chile from nonlocal refugia from the north and east, representing a region of secondary contact between all four glacial lineages. Northwestern glacial relicts likely followed pro-glacial lakes into central Chilean Patagonia, whereas catastrophic changes in drainage direction (Atlantic --> Pacific) for several eastern palaeolakes were the likely avenues for invasions from the east. These mechanisms, combined with evidence for recent, rapid and widespread population growth could explain the extensive contemporary distribution of G. platei throughout Patagonia.

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Changes in lake and stream habitats during the growth and retreat of Pleistocene glaciers repeatedly altered the spatial distributions and population sizes of the aquatic fauna of the southern Andes. Here, we use variation in mtDNA control region sequences to infer the temporal dynamics of two species of southern Andean fish during the past few million years. At least five important climate events were associated with major demographic changes: (i) the widespread glaciations of the mid-Pliocene (c. 3.5 Ma); (ii) the largest Patagonian glaciation (1.1 Ma); (iii) the coldest Pleistocene glaciation as indicated by stacked marine delta(18)O (c. 0.7 Ma); (iv) the last southern Patagonian glaciation to reach the Atlantic coast (180 ka); and (v) the last glacial maximum (LGM, 23-25,000 years ago). The colder-water inhabitant, Galaxias platei, underwent a strong bottleneck during the LGM and its haplotype diversity coalesces c. 0.7 Ma. In contrast, the more warm-adapted and widely distributed Percichthys trucha showed continuous growth through the last two glacial cycles but went through an important bottleneck c. 180,000 years ago, at which time populations east of the Andes may have been eliminated. Haplotype diversity of the most divergent P. trucha populations, found west of the Andes, coalesces c. 3.2 Ma. The demographic timelines obtained for the two species thus illustrate the continent-wide response of aquatic life in Patagonia to climate change during the Pleistocene, but also show how differing ecological traits and distributions led to distinctive responses.

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Thirteen polymorphic microsatellite loci are described for the South American freshwater fish Percichthys trucha. Number of alleles per locus ranged from two to 21 and observed heterozygosities ranged from 0.304 to 0.915 in a sample of 47 individuals from four different sampling locations.

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We used molecular evidence to examine the roles that vicariance mechanisms (mountain-building and drainage changes during the Pleistocene) have played in producing phylogeographical structure within and among South American fish species of the temperate perch family Percichthyidae. The percichthyids include two South American genera, Percichthys and Percilia, each containing several species, all of which are endemic to southern Argentina and Chile (Patagonia). Maximum-likelihood phylogenies constructed using mitochondrial DNA (mtDNA) control region haplotypes and nuclear GnRH3-2 intron allele sequences support the current taxonomy at the genus level (both Percichthys and Percilia form strongly supported, monophyletic clades) but indicate that species-level designations need revision. Phylogeographical patterns at the mtDNA support the hypothesis that the Andes have been a major barrier to gene flow. Most species diversity occurs in watersheds to the west of the Andes, together with some ancient divergences among conspecific populations. In contrast, only one species (Percichthys trucha) is found east of the Andes, and little to no phylogeographical structure occurs among populations in this region. Mismatch analyses of mtDNA sequences suggest that eastern populations last went through a major bottleneck c. 188 000 bp, a date consistent with the onset of the penultimate and largest Pleistocene glaciation in Patagonia. We suggest that eastern populations have undergone repeated founder-flush events as a consequence of glacial cycles, and that the shallow phylogeny is due to mixing during recolonization periods. The area of greater diversity west of the Andes lies outside the northern limit of the glaciers. mtDNA mismatch analysis of the genus Percilia which is restricted to this area suggests a long-established population at equilibrium. We conclude that patterns of genetic diversity in these South American genera have been primarily influenced by barriers to gene flow (Andean orogeny, and to a lesser extent, isolation in river drainages), and by glacial cycles, which have resulted in population contraction, re-arrangement of some watersheds, and the temporary breakdown of dispersal barriers among eastern river systems.

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