Multiple drainage reversal episodes and glacial refugia in a Patagonian fish revealed by sequenced microsatellites

Abstract

The rise of the southern Andes and the Quaternary glacial cycles influenced the landscape of Patagonia, affecting the phylogeographic and biogeographic patterns of its flora and fauna. Here, we examine the phylogeography of the freshwater fish, Percichthys trucha, using 53 sequenced microsatellite DNA markers. Fish (n= 835) were collected from 16 river systems (46 locations) spanning the species range on both sides of the Andes. Eleven watersheds drain to the Pacific, five of which are trans-Andean (headwaters east of Andes). The remaining five drainages empty into the Atlantic. Three analytical approaches (neighbour-joining tree, hierarchical AMOVAs, Structure) revealed evidence of historic drainage reversals: fish from four of the five trans-Andean systems (Puelo, Futalaufquen/Yelcho, Baker, Pascua) exhibited greater genetic similarity with Atlantic draining systems than with Pacific systems with headwaters west of Andes. Present-day drainage (Pacific versus Atlantic) explained only 5% of total genetic variance, while ancestral drainage explained nearly 27% of total variance. Thus, the phylogeographic structure of P. trucha is consistent with episodes of drainage reversal in multiple systems and suggests a major role for deglaciation in the genetic and indeed the geographical distribution of P. trucha in Patagonia. The study emphasizes the significant role of historical processes in the current pattern of genetic diversity and differentiation in a fish from a southern temperate region.

Keywords: Percichthys trucha; drainage reversals; glacial cycles; glacial refugia; phylogeography; sequenced microsatellites.

Figure 1.

Percichthys trucha sampling locations. West of the Andes south of 42° S, where the LGM reached the edge of the continental shelf, P. trucha is present only in locations associated with trans-Andean systems. Insets: sampling locations in the (a) Valdivia, Bueno and Limay/Negro, (b) trans-Andean Puelo, (c) trans-Andean Futalaufquen/Yelcho, and (d) trans-Andean Baker and Pascua systems. (Online version in colour.)

Figure 2.

Neighbour-joining tree representing P. trucha from 16 river systems (46 sampling locations: lakes or rivers) throughout the species distribution in Chile and Argentina. At the broadest scale, the tree distinguishes collections from Pacific draining systems north of 42° S from collections with headwaters east of the Andes that drain into the Atlantic and those that are trans-Andean south of 42° S and drain into the Pacific. Within the first group, collections from Maipo and Nilahue (1 and 2) and to a lesser extent, from the Biobío system (3–5) are distinguishable from those to the south (6–14). Within the second group the colouring reflects two glacial refugia east of Andes, one in northern and one in southern Patagonia. Seven collections have sample sizes n ≤ 2 (electronic supplementary material, table S1), regardless, they cluster within their respective river systems. (Online version in colour.)

Figure 3.

Hierarchical population structure analyses of P. trucha from 16 drainages. Populations are ordered as in the electronic supplementary material, table S1. (a) All sampling locations, K = 2 distinguishing collections from Pacific draining systems north of latitude 42°S versus Atlantic draining systems throughout the species' distribution with those from trans-Andean systems south of 42° S. (b) Genetic differentiation within each of the groupings found in level (a) above. Two groups are distinguished among the collections from the Atlantic draining systems in Argentina and the trans-Andean systems south of 42° S probably reflecting two glacial refugia east of the Andes, in northern southern Patagonia, respectively. Levels (c) and (d), differences among sampling locations within river systems reflecting influence of genetic drift. Within (c) the Baker system (samples 32–41) is distinguishable from Chalia, Pascua and Santa Cruz systems (samples 42–46). Differences among these sampling locations become apparent in (d). Lake San Martin (43), drains into both the Atlantic and Pacific. (Online version in colour.)