Contrasting Patterns of Genetic Diversity and Divergence Between Landlocked and Migratory Populations of Fish Galaxias maculatus, Evaluated Through Mitochondrial DNA Sequencing and Nuclear DNA Microsatellites

Abstract

Galaxias species are interesting biogeographic models due to their distribution and different types of life cycles, with migratory and landlocked populations. To obtain a better understanding of the genetic consequences of the Quaternary glacial cycles in Galaxias maculatus, in this work we compared landlocked and migratory populations collected in areas that were differentially affected by ice advances and retreats. We included nine populations of G. maculatus, four collected from lakes (landlocked) and five from their associated estuaries/rivers (migratory) in three estuary-lake systems across southern Chile. Genetic analyses were performed using the mitochondrial control region and nine microsatellite loci. Genetic diversity measured with both markers was significantly higher in migratory than in landlocked populations across the study area. The levels of genetic differentiation showed higher differentiation among lakes than estuaries. Genetic diversity was higher in migratory populations located in areas that were less impacted by ice during Quaternary glacial processes. These results may be the consequence of recent recolonization of small freshwater bodies following the Last Glacial Maximum (LGM). Finally, the greatest differentiation was observed in populations that were exposed to continental ice advances and retreats during the LGM. Thus, in the present work we corroborate a pattern of differentiation between lakes and estuaries, using mtDNA sequences and microsatellite nuclear markers. This pattern may be due to a combination of biological factors, i.e., resident non-migratory behaviour or landlocking and natal homing-in, as well as geological factors, i.e., Expansion-Contraction Quaternary glacial biogeographic processes.

Keywords: Chile; estuary; lake; last glacial maximum; mtDNA.

FIGURE 1

Map showing Galaxias maculatus sampling locations in western Patagonia separated into the three systems analysed.

FIGURE 2

Maximum parsimony haplotype networks in Galaxias maculatus based on mtDNA D-loop sequences from: (A) Estuary-Lake System 1: E-LS 1 (Moncul Estuary: Mon E, Lingue Estuary: Lin E and Colico Lake: Col L); (B) Estuary-Lake System 2: E-LS 2(Maullín Estuary: Mau E, Llanquihue Lake: Llan L and Pichilaguna Lake: Pic L); and (C) Estuary-Lake System 3: E-LS3 (Tortel Estuary: Tor E, Pascua Estuary: Pas E and Quetru Lake: Que L). Each haplotype is represented by a coloured circle showing the locality where it was collected. The size of the circles is proportional to the frequency in the sampling effort.

FIGURE 3

Genetic differentiation between locations, assessed by Bayesian analysis: (A) Diagram of the estimated population structure of Galaxias maculatus for the nine locations sampled with K = 2, the colours represent the genetic groups; (B) Diagram of population structure with K = 5. The name of the localities is observed on the lower horizontal axis: MON-E: Moncul Estuary; LIN-E: Lingue Estuary; COL-L: Colico Lake; MAU-E: Maullín Estuary; LLA-L: Llanquihue Lake; PIC-L Pichilaguna Lake; TOR-E: Tortel Estuary; PAS-E: Pascua Estuary and QUE-L Quetru Lake.

FIGURE 4

Ordering of the Galaxias maculatus clusters identified by the discriminant analysis of principal components (DAPC) of the different locations sampled. 1) Quetru Lake (QUE-L); 2: Pichilaguna Lake (PIC-L); 3: Lingue Estuary (LIN-E); 4: Colico Lake (COL-L); 5: Llanquihue Lake (LLA-L); 6: Maullín Estuary (MAU-E); 7: Moncul Estuary (MON-E)—Tortel Estuary (TOR-E)- Pascua Estuary (PAS-E).