Are There Barriers Separating the Pink River Dolphin Populations (Inia boliviensis, Iniidae, Cetacea) within the Mamoré-Iténez River Basins (Bolivia)? An Analysis of Its Genetic Structure by Means of Mitochondrial and Nuclear DNA Markers

Abstract

The pink river dolphin, or bufeo, is one of the dolphins which lives in the rivers of the Orinoco and Amazon basins in South America. The Bolivian bufeo population is considered a differentiated species (Inia boliviensis) from the Amazon and Orinoco species (Inia geoffrensis). Until now, no study has completed an extensive population genetics analysis of the bufeo in Bolivian rivers. We analyzed 82 bufeos from different rivers from the Mamoré and Iténez (Guaporé) river basins for the mt control region (CR), nuclear microsatellites, and DQB-1 gene sequences to determine if the inner rapids of these Bolivian river basins have some influence on the genetic structure of this species. The first relevant result was that the genetic diversity for CR, and the microsatellites were substantially lower in the Bolivian bufeos than in the dolphins studied in other areas of the Amazon and Orinoco. However, the DQB-1 gene sequences yielded similar genetic diversity to those found in other areas. The second relevant result is the existence of some significant genetic heterogeneity among the bufeo populations within Bolivia, although in a small degree, but this differentiation is independent of the inner rapids of the Bolivian rivers we sampled. The third relevant result was the existence of significant isolation by distance for the CR, but not for microsatellites and DQB-1 gene sequences. This was related to differential gene flow capacity of females (philopatric) and males (less philopatric and more migrants) and, possibly, to different selective patterns affecting the molecular markers studied. The fourth relevant result was related to diverse demographic changes of these bufeos. At least two or three bottleneck events and one or two population expansions have occurred in the Bolivian bufeo population. The major part of these events occurred during the Pleistocene.

Keywords: DQB-1 gene sequences; Inia boliviensis; Pleistocene; South American climatic and geological changes; microsatellites; mitochondrial control region; rapids; spatial patterns.

Figure 1

Map with the 10 Inia boliviensis populations sampled in the Mamoré and Iténez (Guaporé) rivers (Bolivia) for different molecular markers. Pop 1 = four sampling points (Porvenir, Bellaunión, Cerrito, and Iruyañez River mouth), all in the Mamoré River; Pop 2 = Bolivar (Mamoré River); Pop 3 = El Corte (Mamoré River); Pop 4 = El Azul (Iténez River); Pop 5 = San Martín River (Iténez River); Pop 6 = Securé River (Mamoré River); Pop 7 = Ibaré River (Mamoré River); Pop 8 = Tijamuchí River (Mamoré River); Pop 9 = Ipurupuru River (Iténez River); Pop 10 = mouth of Ibaré River with Mamoré River. The rapids in the Mamoré River are also shown on the map.

Figure 2

Maximum likelihood tree showing the relationships among 82 bufeos (Inia boliviensis) sampled in Bolivian rivers sequenced at the mt control region. The number in the nodes are the bootstrap percentages.

Figure 3

Different populations of bufeos (I. boliviensis) detected by means of BAPS in Bolivian rivers for the mt Control Region with 82 bufeo specimens; three populations were detected.

Figure 4

Correspondence factorial analysis showing the relationships of 61 bufeos (I. boliviensis) analyzed for 10 DNA microsatellites in Bolivian rivers. The specimens sampled in the Iténez (Guaporé) River were the most differentiated.

Figure 5

Different populations of bufeos (Inia boliviensis) detected by means of BAPS in Bolivian rivers using 10 DNA microsatellite markers. (A) Sixty-one specimens assuming no admixture among different localities; six populations were detected. (B) Sixty-one specimens assuming admixture among different localities; six populations were detected. (C) Eight populations assuming no admixture among them; three populations were detected. (D) Eight populations assuming admixture among them; one population was detected. Each different color indicates a different population.

Figure 6

Minimum evolution tree with the Kumar tree analyzing DQB-1 gene sequences in bufeos (I. boliviensis) sampled in Bolivian rivers. This three shows the relationship among the 11 DQB-1 alleles found in the Bolivian rivers and those found in Inia populations from the Peruvian Amazon rivers and from the Orinoco (Colombian and Venezuelan) basin rivers.

Figure 7

Different populations of bufeos (I. boliviensis) detected by means of BAPS in Bolivian rivers using DQB-1 gene sequences. Twenty-three (23) specimens were analyzed, and four populations were detected.

Figure 8

Mantel test between the geographic and genetic distances for specimens of bufeos (I. boliviensis) sampled in Bolivian rivers for 82 specimens at the mt control region. Significant spatial structure was found.

Figure 9

Correlogram with the Ay statistic and five distance classes from a spatial autocorrelation analysis for bufeos (I. boliviensis) in the Bolivian rivers for 82 specimens at the mt control region. Significant isolation by distance was detected.

Figure 10

Distograms using five distance classes to analyze the spatial genetic structure of the bufeo (I. boliviensis) in the Bolivian rivers at the mt control region. (A) For the haplotypes found using the Gregorious distance [96]. (B) For the haplotypes found using haplotypes in common. No significant pattern was found with these procedures.

Figure 11

Genetic-landscape interpolation analysis (GLIA) for bufeos (I. boliviensis) across Bolivian rivers for 82 specimens analyzed at the mt control region. Isolation by distance and genetic patches were detected with this procedure. The color gradient shows the isolation by distance, meanwhile the peaks indicate some genetic patches.

Figure 12

Mantel test between the geographic and genetic distances for specimens of bufeos (I. boliviensis) sampled in Bolivian rivers. Sixty-one (61) specimens analyzed at 10 DNA microsatellites. No spatial structure was found with DNA microsatellites.

Figure 13

Correlogram with the Ay statistic and five distance classes from a spatial autocorrelation analysis for bufeos (I. boliviensis) in the Bolivian rivers at 10 DNA microsatellite markers. Sixty-one (61) specimens were analyzed for this procedure. No spatial structure was found with DNA microsatellites. In fact, the most nearby specimens were the most differentiated ones.

Figure 14

Genetic-landscape interpolation analysis (GLIA) for bufeos (I. boliviensis) across Bolivian rivers at 10 DNA microsatellite markers. Sixty-one (61) specimens analyzed for this procedure. No clear genetic patches were detected with this technique.

Figure 15

Median-joining network (MJN) with haplotypes identified in 82 specimens of bufeos (I. boliviensis) sampled in Bolivian rivers at the mt control region. Green = Pop 1; pink = Pop 2; orange = Pop 3; light blue = Pop 4; lilac = Pop 5; light green = Pop 6; dark blue = Pop 7; brown = Pop 8; red = Pop 9; yellow = Pop 10; black = Pontoporia blainvillei (outgroup). Small red circles indicate missing intermediate haplotypes.

Figure 16

Bayesian skyline plot analyses (BSP) to determine possible demographic changes across the natural history of bufeos (I. boliviensis) in Bolivian rivers with (A) mt control region in the last 400,000 years and (B) with mt control region in the last 17,500 years. Population declination was observed during the last phase of the Pleistocene and a light population increase was detected in the recent centuries.