“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

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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.).

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  • Bangor University

    Bangor University has a long record of academic excellence and a reputation for excellent teaching and student care. The University has 11,000 students and offers 500 degree programmes, with particular strengths in the fields of Environmental Science (including Ocean Sciences), Health (including Psychology, Neuroscience and Sports Science), Humanities, Physical Sciences, Business, Law, Social Sciences and Education. With 2,000 members of staff, Bangor University is a major employer in north Wales and a leading contributor to the regional economy.

    Research at Bangor University has been highly rated. The 2014 Research Excellence Framework recognised over three-quarters of Bangor’s research as either “world-leading” or “internationally excellent”. The University retains its leads in Wales and its position in the top 10 in the UK (of the UK’s best non-specialist universities, the traditional institutions who offer a broad range of subjects) in the annual National Student Survey (2015).

  • The University of Bristol

    The University of Bristol is one of the most popular and successful universities in the UK. It was ranked within the top 40 universities in the world in the QS World University rankings 2015 and 9th in the country. The University of Bristol is ranked among the top five institutions in the UK for its research, according to new analysis of the Research Excellence Framework (REF) 2014.

    Bristol is a member of the Russell Group of UK research-intensive universities, and a member of the Worldwide Universities Network, a grouping of research-led institutions of international standing.

    The University was founded in 1876 and was granted its Royal Charter in 1909. It was the first university in England to admit women on the same basis as men.

    The University is a major force in the economic, social and cultural life of Bristol and the region, but is also a significant player on the world stage. It has over 16,000 undergraduates and nearly 6,000 postgraduate students from more than 100 countries, and its research links span the globe.

    Twelve Bristol graduates and members of staff have been awarded Nobel Prizes, including Sir Winston Churchill who was Chancellor of the University of Bristol from 1929 until 1965.

  • The Wellcome Trust/ Cancer Research UK Gurdon Institute, University of Cambridge

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    Institute scientists use a range of model systems such as yeast, nematode worms, fruit flies, frogs, mammalian cells and organoids to study development and disease at the level of molecules, cells and tissues.

    Research conducted at the Institute has so far led to nine spin-out companies (including KuDOS Pharmaceuticals, Abcam, Chroma Therapeutics, CellCentric, MISSION Therapeutics and Talisman Therapeutics) and five candidate drugs. One of these, olaparib (Lynparza), has been approved in the UK, Europe and the USA for use against ovarian cancers.

  • The Wellcome Trust Sanger Institute

    The Wellcome Trust Sanger Institute is one of the world’s leading genome centres. Through its ability to conduct research at scale, it is able to engage in bold and long-term exploratory projects that are designed to influence and empower medical science globally. Institute research findings, generated through its own research programmes and through its leading role in international consortia, are being used to develop new diagnostics and treatments for human disease.

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  • Wellcome Trust Mathematical Genomics and Medicine (MGM) PhD programme, University of Cambridge