Geographical differentiation of the Euchiloglanis fish complex (Teleostei: Siluriformes) in the Hengduan Mountain Region, China: Phylogeographic evidence of altered drainage patterns

Abstract

The uplift of the Tibetan Plateau caused significant ecogeographical changes that had a major impact on the exchange and isolation of regional fauna and flora. Furthermore, Pleistocene glacial oscillations were linked to temporal large-scale landmass and drainage system reconfigurations near the Hengduan Mountain Region and might have facilitated speciation and promoted biodiversity in southwestern China. However, strong biotic evidence supporting this role is lacking. Here, we use the Euchiloglanis fish species complex as a model to demonstrate the compound effects of the Tibetan Plateau uplift and Pleistocene glacial oscillations on species formation in this region. The genetic structure and geographical differentiation of the Euchiloglanis complex in four river systems within the Hengduan Mountain Region were deduced using the cytochrome b (cyt b) gene and 10 microsatellite loci from 360 to 192 individuals, respectively. The results indicated that the populations were divided into four independently evolving lineages, in which the populations from the Qingyi River and Jinsha River formed two sub-lineages. Phylogenetic relationships were structured by geographical isolation, especially near drainage systems. Divergence time estimation analyses showed that the Euchiloglanis complex diverged from its sister clade Pareuchiloglanis sinensis at around 1.3 Million years ago (Ma). Within the Euchiloglanis complex, the divergence time between the Dadu-Yalong and Jinsha-Qingyi River populations occurred at 1.0 Ma. This divergence time was in concordance with recent geological events, including the Kun-Huang Movement (1.2-0.6 Ma) and the lag time (<2.0 Ma) of river incision in the Hengduan Mountain Region. Population expansion signals were detected from mismatched distribution analyses, and the expansion times were concurrent with Pleistocene glacier fluctuations. Therefore, current phylogeographic patterns of the Euchiloglanis fish complex in the Hengduan Mountain Region were influenced by the uplift event of the Tibetan Plateau and were subsequently altered by paleo-river transitions during the late Pleistocene glacial oscillations.

Keywords: Euchiloglanis; Hengduan Mountain Region; Pleistocene glacial oscillations; genetic structure; phylogeny; phylogeography.

Figure 1

Dorsal and ventral view of the Euchiloglanis. The specimen was caught in the Dadu River, China

Figure 2

Sampling locations for Euchiloglanis in Hengduan Mountain Region. Different sites were colored according to the structure clusters. Location codes were consistent with those showed in Table 1

Figure 3

Scatter plots of genetic distance vs. geographical distance (km: kilometer) for pairwise population comparisons inferred from cyt b (a) and microsatellite data (b)

Figure 4

Phylogenetic relationships based on cyt b haplotypes. Numbers represented nodal supports inferred from Bayesian posterior probability (BI), neighbor‐joining probability (NJ), and maximum parsimony bootstrap analyses (MP), respectively. The supported or bootstrap value was only displayed among main clades. The symbol of “*” indicated a well‐supported Bayes posteriori possibility that reached a level of 1.0 or a significant bootstrap level of 100. Glyptosternon maculatum was used as an outgroup. Different colors do indicating different geographical locations

Figure 5

Median‐joining network of haplotypes identified in the cyt b. Haplotype numbers are consistent with those showed in Table S1. Circle sizes indicated the approximate numbers of individuals. Red dots represented number of nucleotide substitutions between haplotypes. Different colors indicated different geographical locations

Figure 6

Structure clustering conducted based on microsatellite loci within populations of Euchiloglanis. (a) Delta K as a function of the K values according to 20 run outputs and (b) structure results at K = 4, with different colors indicating different clusters

Figure 7

Divergence time estimation with time‐calibrated points was reconstructed from cyt b sequence. Digital numbers up branches indicated the time of species divergence events occurred (Ma: million years ago), following with the 95% credibility interval. Bayesian posterior probability was placed under divergence time labels

Figure 8

Mismatch distributions (left) and Bayesian skyline plots (right) of five population groups of Euchiloglanis inferred from mtDNA cyt b sequences. The Dadu River groups were analyzed according to sampled populations of JC, DB, and MEK. The Yalong River was computed based on the sampled populations of YJ, XL, DF, and GZ. The third group was calculated based on the sampled populations of BZL and DW. The other two groups were calculated based on the population of LB and TQ, respectively. For Bayesian skyline plots, the x‐axes were the time scale in million years, and the y‐axes were effective population size (units = Ne *τ, Ne represents the effective population size, τ represents generational time of the organism), the black line depicts the median population size, and the shaded areas represented the 95% confidence intervals of HPD analysis