Discordant population histories of host and its parasite: A role for ecological permeability of extreme environment?

Dagmar Jirsová,Miloslav Jirků,Jan Štefka,Heike Lutermann

doi:10.1371/journal.pone.0175286

Abstract

Biogeographical and ecological barriers strongly affect the course of micro-evolutionary processes in free living organisms. Here we assess the impact of a recently emerged barrier on populations of limnic fauna. Genetic diversity and population structure in a host-parasite system (Wenyonia virilis tapeworm, Synodontis schall catfish) are analyzed in the recently divided Turkana and Nile basins. The two basins, were repeatedly connected during the Holocene wet/dry climatic oscillations, following late Pleistocene dessication of the Turkana basin. Mitochondrial DNA sequences for cytochrome oxidase I gene (cox I) and a whole genome scanning method—amplified fragment length polymorphism (AFLP) were employed. A total of 347 cox I sequences (representing 209 haplotypes) and 716 AFLP fragments, as well as 120 cox I sequences (20 haplotypes) and 532 AFLP fragments were obtained from parasites and hosts, respectively. Although results indicate that host and parasite populations share some formative traits (bottlenecks, Nilotic origin), their population histories/patterns differ markedly. Mitochondrial analysis revealed that parasite populations evolve significantly faster and show remarkably higher genetic variability. Analyses of both markers confirmed that the parasites undergo lineage fission, forming new clusters specific for either freshwater or saline parts of Lake Turkana. In congruence with the geological history, these clusters apparently indicate multiple colonisations of Lake Turkana from the Nile. In contrast, the host population pattern indicates fusion of different colonisation waves. Although fish host populations remain connected, saline habitats in Lake Turkana (absent in the Nile), apparently pose a barrier to the gene flow in the parasite, possibly due to its multihost lifecycle, which involves freshwater annelids. Despite partially corroborating mitochondrial results, AFLP data was not sufficiently informative for analyzing populations with recently mixed biogeographic histories.

Highlights

The cyclic Pleistocene climatic oscillations severely affected all biomes
Principal Coordinate Analysis (PCoA) clustering of individuals did not corroborate the separation of W. virilis specimens into mtDNA haplogroups, but showed some differentiation between the Turkana and Nile populations (Fig 5a and 5b)
The AMOVA analyses based on FST calculation (Infinite Alleles Model) revealed that the majority of variation occurred within the sample sites for all datasets (90% for parasite, 93% for host in the whole dataset; 89% for the parasite, 98% for the host in Lake Turkana dataset)

Summary

Introduction

The cyclic Pleistocene climatic oscillations severely affected all biomes. Alternating hot-humid and cool-dry periods lasting for tens of millennia caused repeated contraction/expansion and/ or fragmentation of vegetational belts and hydrological systems [1]. Freshwater habitats and taxa were among the most severely affected [2,3,4]. Contractions/fragmentations of hydrological systems during the cold-dry periods resulted in patchy distribution of limnic biota, which remained restricted to areas with continuous freshwater habitats. In the tropics such humid refugia allowed localized persistence and accumulation of both aquatic and terrestrial taxa during the critical cold-dry periods and these are recognized as biodiversity and/or endemism centres analogous to the Pleistocene refugia of the Holarctic [4,5]. The significance of African Pleistocene refugia for speciation processes remains unclear, since many of the radiations associated with them are of Miocene or older ages The significance of African Pleistocene refugia for speciation processes remains unclear, since many of the radiations associated with them are of Miocene or older ages (African vertebrates: phylogenetic evidence e.g. [6,7,8]; indirect paleontological evidence e.g. [9,10]) and because there is only limited information available on millennial-scale genetic processes in metazoans [11,12]

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Discussion

Conclusion