Population structure and microscale morphological differentiation in a freshwater snail from the Chilean Altiplano

Abstract

Background: The diversity and population genetic structure of many species have been shaped by historical and contemporary climatic changes. For the species of the South American Altiplano, the historical climatic changes are mainly related to the wet events of great magnitude and regional influence that occurred during the Pleistocene climatic oscillations (PCOs). In contrast, contemporary climate changes are associated with events of lesser magnitude and local influence related to intensifications of the South American Summer Monsoon (SASM). Although multiple studies have analyzed the effect of PCOs on the genetic patterns of highland aquatic species, little is known about the impact of contemporary climate changes in recent evolutionary history. Therefore, in this study, we investigated the change in population structure and connectivity using nuclear and mitochondrial markers throughout the distribution range of Heleobia ascotanensis, a freshwater Cochliopidae endemic to the Ascotán Saltpan. In addition, using geometric morphometric analyses, we evaluated the concomitance of genetic divergence and morphological differentiation.

Results: The mitochondrial sequence analysis results revealed the presence of highly divergent co-distributed and geographically nested haplotypes. This pattern reflects an extension in the distribution of groups that previously would have differentiated allopatrically. These changes in distribution would have covered the entire saltpan and would be associated with the large-scale wet events of the PCOs. On the other hand, the microsatellite results defined five spatially isolated populations, separated primarily by geographic barriers. Contemporary gene flow analyses suggest that post-PCO, climatic events that would have connected all populations did not occur. The morphometric analyses results indicate that there is significant morphological differentiation in the populations that are more isolated and that present the greatest genetic divergence.

Conclusions: The contemporary population structure and morphological variation of H. ascotanensis mainly reflect the post-PCO climatic influence. Although both markers exhibit high genetic structuring, the microsatellite and morphology results show the preponderant influence of fragmentation in recent evolutionary history. The contemporary genetic pattern shows that in species that have limited dispersal capabilities, genetic discontinuities can appear rapidly, erasing signs of historical connectivity.

Keywords: Aquatic invertebrate; Fragmentation; Geometric morphometrics; Pleistocene climatic oscillations; South American summer monsoon.

Fig. 1

Sampling localities of Heleobia ascotanensis used in the present study. A Map showing the Ascotán Saltpan and the 13 springs analyzed. B Detail of springs 2 to 6. C and D correspond to photographs of springs 2 and 9, respectively. Each photograph shows representative individuals of each population (the black circle represents 5 mm). All photographs by Moisés A. Valladares. The map was made using QGIS Geographic Information System v3.4.9 with ESRI world imagery (ESRI, DigitalGlobe, GeoEye, Earthstar Geographics, CNES/Airbus DS, USDA, USGS, AeroGRID, IGN, and the GIS User Community) (http://www.qgis.org, accessed on April 10, 2023)

Fig. 2

Haplotype network of Heleobia ascotanensis from the Ascotán Saltpan generated using COI gene sequences. The segments on the lines represent the number of mutational steps. The size of the circumferences represents the relative frequency of each haplotype. A, B, D and E indicate divergent haplotypes, and C indicates the higher-frequency haplotype (details in main text)

Fig. 3

Population structure of Heleobia ascotanensis from 10 microsatellite loci using a hierarchical Structure analysis

Fig. 4

Estimated migration rates for Heleobia ascotanensis populations from 10 microsatellite loci in the Ascotán Saltpan. The groupings correspond to the populations defined by Structure. Rates greater than 2% are indicated, and the self-recruitment rate is highlighted in bold

Fig. 5

Morphological differentiation associated with shell size among Heleobia ascotanensis populations. Differences of the logarithm of the size of the centroid classifying the individuals according to the populations defined by Structure. The population mean of the centroid size is shown, and significant differences are indicated (Bonferroni post hoc)

Fig. 6

Morphological space of the populations of Heleobia ascotanensis. Principal component analysis using the GPA matrix of the populations defined by Structure. The deformation grids for the extreme shapes of each axis of variation in relation to the global consensus are shown in the corners of the graph