Amassing diversity in an ancient lake: evolution of a morphologically diverse parthenogenetic gastropod assemblage in Lake Malawi

Abstract

Exceptional ecological niche diversity, clear waters and unique divergent selection pressures have often been invoked to explain high morphological and genetic diversity of taxa within ancient lakes. However, it is possible that in some ancient lake taxa high diversity has arisen because these historically stable environments have allowed accumulation of lineages over evolutionary timescales, a process impossible in neighbouring aquatic habitats undergoing desiccation and reflooding. Here we examined the evolution of a unique morphologically diverse assemblage of thiarid gastropods belonging to the Melanoides polymorpha'complex' in Lake Malawi. Using mitochondrial DNA sequences, we found this Lake Malawi complex was not monophyletic, instead sharing common ancestry with Melanoides anomala and Melanoides mweruensis from the Congo Basin. Fossil calibrations of molecular divergence placed the origins of this complex to within the last 4 million years. Nuclear amplified fragment length polymorphism markers revealed sympatric M. polymorpha morphs to be strongly genetically differentiated lineages, and males were absent from our samples indicating that reproduction is predominantly parthenogenetic. These results imply the presence of Lake Malawi as a standing water body over the last million years or more has facilitated accumulation of clonal morphological diversity, a process that has not taken place in more transient freshwater habitats. As such, the historical stability of aquatic environments may have been critical in determining present spatial distributions of biodiversity.

Old fossils–young species: evolutionary history of an endemic gastropod assemblage in Lake Malawi

“…Second, Lanistes and Melanoides from Lake Malawi might also differ in their geographical origin. Genner et al (2007b) suggested a possible origin of the Melanoides polymorpha complex west of the rift, e.g. in a shared watershed of the Congo-Zambezi.…”

Lacustrine mollusc radiations in the Lake Malawi Basin: experiments in a natural laboratory for evolution

“…They are not yet present in Chiwondo times and may be dwarfed morphs that originated during Pleistocene times in the saline lakes, but that these morphs are descended from populations already present in the basin during Chiwondo times (Genner et al, 2007b) cannot be ascertained. The dominant fossil Chiwondo Melanoides was identified as M. cf.…”

“…Presently it seems best to consider them to belong to the M. polymorpha-M. mweruensis-M. anomala species group, occurring in the south-eastern African region . Using these Chiwondo fossils to calibrate the molecular clock in calculating the age of the modern M. polymorpha-group should be avoided (Genner et al, 2007b).…”

“…Eldblom and Kristensen (2003) retain three endemics only in the last revision based on morphology. While molecular biologists speak of the "Melanoides polymorpha-complex", considered to be a poly-or paraphyletic group of clones (Genner et al, 2004(Genner et al, , 2007bVon Gersdorff Sørensen et al, 2005). This led Michel et al (2008) to raise a question about their equivalence to "standard" species, i.e., as defined according to the Biological Species Concept (BSC).…”

“…Both these Malawi species groups are monophyletic, young and the speciation processes still likely are going on in the viviparid flock (Schultheiß et al, 2011). In addition, the possibility that the clonal Melanoides lineages endemic to lake Malawi are not the result of an in-lake radiation either, but that they are allopatric paleo-endemics that colonized Lake Malawi at different times, is considered a possible scenario in view of their para-/polyphyly (Genner et al, 2007b). Dudley's (2000) remark that "Malawi gastropod classification is in a continuing state of revision and that it will be some time before a system comes to be generally agreed for the groups of higher rank" is still painfully actual.…”