Speciation patterns and processes in the zooplankton of the ancient lakes of Sulawesi Island, Indonesia

Abstract

Although studies of ancient lake fauna have provided important insights about speciation patterns and processes of organisms in heterogeneous benthic environments, evolutionary forces responsible for speciation in the relatively homogenous planktonic environment remain largely unexplored. In this study, we investigate possible mechanisms of speciation in zooplankton using the freshwater diaptomids of the ancient lakes of Sulawesi, Indonesia, as a model system. We integrate phylogenetic and population genetic analyses of mitochondrial and nuclear genes with morphological and genome size data. Overall, our results support the conclusion that colonization order and local adaptation are dominant at the large, island scale, whereas at local and intralacustrine scales, speciation processes are regulated by gene flow among genetically differentiated and locally adapted populations. In the Malili lakes, the diaptomid populations are homogenous at nuclear loci, but show two highly divergent mitochondrial clades that are geographically restricted to single lakes despite the interconnectivity of the lake systems. Our study, based on coalescent simulations and population genetic analyses, indicates that unidirectional hybridization allows gene flow across the nuclear genome, but prevents the introgression of mitochondria into downstream populations. We suggest that hybridization and introgression between young lineages is a significant evolutionary force in freshwater plankton.

Keywords: Ancient lakes; Malili lakes; copepoda; plankton; population structure.

Figure 1

(A) A map of sampling sites across Sulawesi, Indonesia. The dashed arrows indicate the direction of water flow. The Bayesian (BI) phylogeny for the cytochrome c oxidase subunit I (COI) gene (B) shows two divergent mitochondrial lineages inhabiting Lake Tondano and two in the Malili lakes. These lineages collapse in the BI phylogeny for the ITS1 region (C) suggesting that hybridization has homogenized the ribosomal genes. Numbers in parentheses indicate the number of sampled individuals within the clade or haplotype. Node supports are BI posterior probabilities followed by neighbor-joining bootstrap values.

Figure 2

Maximum parsimony haplotype network for the cytochrome c oxidase subunit I (COI) gene. Colored circles represent haplotypes, with size corresponding to haplotype frequency. Single lines correspond to single mutation steps (i.e., 1 base pair change) and small open circles represent extinct or unsampled haplotypes.

Figure 3

Proposed model for restricted gene flow between populations of the two Malili clades. White and gray bodies represent MA/MH and TO nuclear genomes, respectively, and white and black circles represent MA/MH and TO mitochondria, respectively. The maternal lineage of migrants (gray box) will suffer hybrid breakdown as their mitochondria find themselves in an ever-increasing divergent nuclear background after repeated backcrossing. All other hybrid crosses will regain native mitochondria and progressively disseminate migrant genes into the population with each backcross.