Matt McGee, first author of the study and professor at Monash University in Australia, and Joana Meier, co-author of the study and Bateson Research Fellow at St. John's College, Cambridge. They were both postdocs, and Joana Meier was also a PhD student with Ole Seehausen at Eawag and the University of Bern.

Representative sample

In previous studies, Seehausen’s group showed that the rapid cichlid radiation was due to the earlier hybridisation of two distantly related lineages, which came into contact again around 150,000 years ago after several million years of geographical separation; subsequently, their descendants are believed to have been repeatedly isolated and brought together again in hybrid swarms during the turbulent period leading up to the formation of Lake Victoria and its modern fauna.

In the latest study, the researchers analysed the genomes of 100 cichlid species from the Lake Victoria radiation, representing all the various genera, feeding habits and morphologies. This data was compared with genomic data from 20 slowly or less rapidly speciating cichlids from eight other lakes, and with literature/digital repository data on all known cichlid species.

Indels in the spotlight

The new data showed a positive correlation between the speciation rate and the number of indels found in the genome. Indels are short DNA sequences containing base pair insertions or deletions, which may be absent in one species while one or more copies are present in closely related species; they are more difficult to detect than base pair replacements (i.e. point mutations) and have tended to play a minor role in evolutionary theory to date.

The researchers found thousands of indels between the genomes of any two species in the rapidly speciating Lake Victoria flock,. In the “slower” lineages from other lakes, the density of indels in the genome that had accumulated between species per unit time was lower; they had evidently accumulated more slowly – and the rate of speciation was correspondingly slower.

“Use it or lose it” potential

Investigations of the function of Lake Victoria indels revealed that they were significantly associated, in many cases, with variation in diet, habitat and male nuptial coloration. This means that the Lake Victoria cichlids could draw on an indel pool which was not only large but also contained variants important for speciation – directly, through mate choice, or indirectly, through specialisations enabling the fish to occupy new ecological niches. Many of these indels are much older than Lake Victoria or its cichlids and probably arrived in the common ancestor of the radiation through ancient hybridization with other cichlids. Together with the many point mutations that were brought together by ancient hybridisation too, an enormous genomic potential arose.

In a homogeneous environment, this potential would probably soon have disappeared; if genomic variants are not used, they are easily lost – either through chance or uniform selection pressure. But over the last 15,000 years, the large new Lake Victoria evidently offered a wide variety of ecological opportunities and, at a stroke, the fish were able to utilise hundreds of different variants for new – sometimes highly complex – specialisations.

For example, some specialised in scraping firmly attached algae from rocks in clear water close to the shore, while others developed an acute visual capacity enabling them to prey on other fish in the murky deep waters – thanks to gene variants that had been selected much earlier for these specialisations, copies of which were available “ready for use” by young species after the hybridisation.

As these genomic variants facilitated vital specialisations, complementary sets were maintained in the different species and could be recombined again after hybridisation, leading to the evolution of further new species.

A new model

Ole Seehausen says: “We’ve started to develop a model which uses networks rather than phylogenetic trees to describe the evolution of new species. In these networks, not only do new genomic variants arise, but new and old genetic material can be exchanged between species for a very long time. As a result, much more genetic material is available for evolution at all times.”

To what extent this model can also be used to explain different speciation rates in other fish is currently being investigated by scientists at Eawag and the University of Bern – for example, with regard to the whitefish radiation which occurred in prealpine lakes after the last ice age.

Cover picture: Matthew McGee et al. , Nature 2020