“Darwin’s puddle” shows how new species can emerge without geographic separation

Cichlid fish from a tiny volcanic crater have been caught in the act of sympatric speciation

Can new species really evolve if there is no physical boundary to drive genetic separation? Physical and genomic evidence from the 700-metre wide volcanic crater Lake Massoko appears to have caught the process in the act.

The results of studying the whole-genome sequences of 146 small fish in a tiny lake in Africa may help answer a decades-long debate among evolutionary biologists. Can a new species evolve if there is no geographic barrier to physically separate the new species from the old (sympatric speciation)? And, if it is possible, what are the genetic and physical traits that drive this form of evolution: sexual attraction, or specialisation in lifestyle, diet or other ecological factors?

“The idea of sympatric speciation has divided evolutionary opinion for a long time. It has been difficult to substantiate that new species can arise when genetic variations can be exchanged easily between the two evolving groups. But we have caught this form of evolution in the act by identifying two different forms of cichlid fish that are separating from each other within a lake that is only 700 metres wide.”

Professor George Turner Senior author from the School of Biological Sciences, Bangor University

Cichlid fish are a valuable model of evolution. In nearby Lake Malawi, many hundreds of cichlid species have been found, differentiated by size, shape, colour, feeding habits and ecological preferences such as living towards the surface of the lake or at the bottom. Because of this vast diversity the lake is known as “Darwin’s Pond”. In contrast Lake Massoko is “Darwin’s puddle”: a much simpler place with many fewer species and fewer factors to drive speciation.

In the lake, researchers discovered two significantly different forms (ecomorphs) of a common species of cichlid fish. One ecomorph – known as littoral – has yellow-green males and lives towards the shores of the lake. The other form – benthic – has dark blue-black males and lives towards the bottom of the lake where the light levels are much lower. There are many other measurable differences between the ecomorphs, for example in body shape, jaws and diet.

These differences are reflected in the genetic differences observed when whole genomes from the two ecomorphs were sequenced and compared. The majority of significant genetic variation lay in a small number of genomic regions associated with sight (such as rhodopsin and other twilight-associated genes), hormone signalling, size and shape.

“One of the most striking characteristics of this diversification is that less than 1 per cent of the genome appears to be involved. Previous expectations were that speciation involved changes across the whole genome. However, in this example of nascent sympatric speciation, we find that the differences are confined to localised regions of the genome – known as genomic islands – that are associated with specific traits.”

Dr Milan Malinsky First author from the Wellcome Trust Sanger Institute, and the Gurdon Institute, University of Cambridge

Confusingly, no single factor – either genetic or physical – seems to separate the two morphs: although they prefer different depths, the yellow and blue fish are frequently found together. One theoretical model for sympatric speciation is that sexual selection can reinforce differences via mate preference. The investigators also carried out mate-choice experiments between the ecomorphs in a controlled laboratory setting and found some differences, but again not enough to explain the separation by themselves.

“We seem to be seeing a complex combination of ecological separation and mate-choice preference that jointly has allowed the two ecomorphs to separate even in the presence of some genetic exchange. These fish have much to tell us.”

Dr Martin Genner Senior author from the School of Biological Sciences, University of Bristol

An exciting prospect is that these findings in a simple system will be relevant to understanding the much richer and more dramatic evolutionary radiation in Lake Malawi and the other African great lakes, and indeed beyond.

“The same genes are found in many species, both in fish and in other vertebrates. So the mechanisms at work in Lake Massoko are likely to have been involved in speciation more widely over history, driving evolution in which species can separate genetically to exploit new ecological niches even when there is no physical separation.”

Dr Richard Durbin A senior author from the Sanger Institute

More information

Funding

This work was funded by Royal Society–Leverhulme Trust Africa Awards AA100023 and AA130107 (M.J.G., B.P.N. and G.F.T.), Wellcome Trust Ph.D. studentship grant 097677/Z/11/Z (M.M.), Wellcome Trust grant WT098051 (S.S. and R.D.), Wellcome Trust and Cancer Research UK core support and a Wellcome Trust Senior Investigator Award (E.A.M.), Leverhulme Trust Research Fellowship RF-2014-686 (M.J.G.), a University of Bristol Research Committee award (M.G.), a Bangor University Anniversary Ph.D. studentship (A.M.T.), and a Fisheries Society of the British Isles award (G.F.T.).