Mountaintops phylogeography: A case study using small mammals from the Andes and the coast of central Chile

Abstract

We evaluated if two sigmodontine rodent taxa (Abrothrix olivacea and Phyllotis darwini) from the Andes and Coastal mountaintops of central Chile, experienced distributional shifts due to altitudinal movements of habitat and climate change during and after the Last Glacial Maximum (LGM). We tested the hypothesis that during LGM populations of both species experienced altitudinal shifts from the Andes to the lowlands and the coastal Cordillera, and then range retractions during interglacial towards higher elevations in the Andes. These distributional shifts may have left remnants populations on the mountaintops. We evaluated the occurrence of intraspecific lineages for each species, to construct distribution models at LGM and at present, as extreme climatic conditions for each lineage. Differences in distribution between extreme climatic conditions were interpreted as post-glacial distributional shifts. Abrothrix olivacea displayed a lineage with shared sequences between both mountain systems, whereas a second lineage was restricted to the Andes. A similar scenario of panmictic unit in the past was recovered for A. olivacea in the Andes, along with an additional unit that included localities from the rest of its distribution. For P. darwini, both lineages recovered were distributed in coastal and Andean mountain ranges at present as well, and structuring analyses for this species recovered coastal and Andean localities as panmictic units in the past. Niche modeling depicted differential postglacial expansions in the recovered lineages. Results suggest that historical events such as LGM triggered the descending of populations to Andean refuge areas (one of the A. olivacea's lineages), to the lowlands, and to the coastal Cordillera. Backward movements of populations after glacial retreats may have left isolates on mountaintops of the coastal Cordillera, suggesting that current species distribution would be the outcome of climate change and habitat reconfiguration after LGM.

Fig 1. Sampling localities in central Chile.

Map showing the localities sampled in central Chile, from the coast, central valley and Andean areas.

Fig 2. Maximum likelihood (ML) and Bayesian inference (BI) haplotype trees based on D-LOOP sequences of Phyllotis darwini and Abrothrix olivacea.

Haplotype phylogenetic trees representing the intraspecific relationships of Phyllotis darwini and Abrothrix olivacea from central Chile mountaintop and lowland areas. Numbers on the nodes represent the posterior probability and 1,000 bootstrap support values. Color labels on the trees represent mountaintop and/or lowland haplotypes as specified inside the figure. Outgroup for the phylogenies are recovered at the bottom of each phylogeny represented by Phyllotis magister and Abrothrix olivacea tarapacensis. For P. darwini A = lineage A (coastal and Andean), B = lineage B (coastal and Andean); For A. olivacea = A = lineage A (Andean), B = lineage B (coastal and valley).

Fig 3. Neighbor-Net of D-LOOP sequence haplotypes of P. darwini and A. olivacea.

Labels for haplotypes on the network are explained inside the figure.

Fig 4. BI and ML haplotype trees based on the combined D-LOOP-FGB sequences for P. darwini and A. olivacea.

The haplotype trees represent the intraspecific relationships of P. darwini and A. olivacea from central Chile mountaintop and lowland areas (see S2 and S3 Tables for the geographic location of haplotypes of A. olivacea and P. darwini, respectively). Numbers on the nodes represent the posterior probability and 1,000 bootstrap support values. Color labels on the trees represent mountaintop and/or lowland haplotypes as specified inside the figure. For P. darwini A = lineage A (coastal and Andean), B = lineage B (coastal and Andean); For A. olivacea = A = lineage A (Andean), B = lineage B (lowlands-Andean and lowlands).

Fig 5. GENELAND analysis with posterior probability isoclines for P. darwini and A. olivacea.

The genetic structuring analysis denotes the extent of genetic landscapes for the two clusters recovered in P. darwini and two clusters for A. olivacea. Coastal and Andean mountaintops are recovered in the figure. To facilitate interpretation, GENELAND output has been cropped, re-scaled and superimposed over the map of central Chile where this study was conducted for A. olivacea. Black dots represent localities analyzed in this study. Regions with the greatest probability of inclusion are indicated in white, whereas lower probabilities are represented in increasingly darker coloring.

Fig 6. Lineage distribution models for A. olivacea and P. darwini.

The figure shows the species distribution models for the present, and the LGM climatic scenarios (rows). Models were built independently for P. darwini and A. olivacea intraspecific lineages (columns). The yellow color represents suitability areas for the lineages, according to the maximum training sensitivity plus specificity logistic threshold; the red areas represent 50% highest logistic probability value observed between the maximum training sensitivity plus specificity logistic threshold, and the maximum logistic probability value for each model.