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Does hybridization facilitate explosive speciation of Lake Baikal amphipods?

Periodic Reporting for period 1 - HybridSpecLBA (Does hybridization facilitate explosive speciation of Lake Baikal amphipods?)

Reporting period: 2022-09-01 to 2024-08-31

What defines the rate of adaptive evolution and speciation? Why do some lineages exist for millions of years with almost no change, like Coelacanth, while others diversify into hundreds of new species in a few hundred thousand years - like famous cichlid fish from African great lakes? This long-debated problem hides the key to understanding mechanisms of biodiversity origin on the Earth.
In this project we investigate the origin of adaptive radiation of amphipods in Lake Baikal. It has brought forward more than 340 species (20% of the world’s freshwater amphipods), making it one of the largest species flocks after the African cichlid radiations, and one of the only large radiations in temperate climates. We aim to understand why Lake Baikal amphipods underwent explosive speciation, while the other seven comparable ancient great lakes are inhabited by less than a few dozens of species. The two strongest limiting factors of speciation are the lack of genetic variation, (it is needed for building new adaptations) and absence of reproductive isolation (which is needed for species separation). Hybridization provides a solution for both problems, and thus is one of the best candidates for the role of speciation catalyzer. In this project we use transcriptomic and genomic datasets to estimate the role of hybridization in formation of Lake Baikal Amphipoda species flock.
We found evidence of ancient hybridisation between two ancestral lineages of Lake Baikal amphipods. Analyzing the selection processes, which followed after the hybridization event, we demonstrated that introgressed genetic material was a subject to natural selection. As expected, some introgressed material turned out to be harmful and was cleared from the genome by purifying selection. However, some introgressed variation was beneficial and participated in formation of new ecological adaptations of hundreds of species. We suggest that introgressed variation was specifically used for the formation of deepwater adaptations. This scenario is also supported by the history of the group, as Lake Baikal provides diverse oxygenated habitats at depths of up to 1,642 meters for adaptive radiation. These habitats were novel for the ancestral riverine species, but according to our hypothesis, hybridization with another lineage may have helped it to diversify into hundreds of new species and to populate deepwater habitats.
Beside the input into ongoing study of ancient hybridization, our project laid the foundation for making large multi-species genome alignment of Lake Baikal amphipods. We sequenced two reference quality genomes, which represent two independent invasions of amphipods into Lake Baikal. In addition, we sequenced draft genomes of 15 species, which include a huge diversity of ecological specializations: herbivores, carnivores, scavengers, detritophages and parasites. For further development of the project we made a collection of more than a thousand of highly-preserved specimens, which belong to at least a hundred of different species. We expect genome-based alignments to provide a rare high-quality material for the study of speciation processes, comparable to those available for African cichlids.
Finally, we have taken high resolution photographs of Lake Baikal Amphipoda species, which now are available at the project’s website: https://spikesandbristles.pictures(opens in new window). Combined with species descriptions, our website is aimed to help with species identification in the field and to share our appreciation of the stunning beauty of Lake Baikal amphipods.
As fundamental research, our project enhances global understanding of the evolutionary genomic forces that shape biodiversity. We found evidence of ancient introgression and complex signatures of selection on introgressed material in Lake Baikal amphipods. Being added to similar evidence from African cichlid fish and many other species flocks, it shows that the overall phenomenon is widespread and may be characteristic for fast speciation events. This finding raises new questions about the mechanisms underlying adaptive evolution. Our future research aims to validate these findings through extended genome-based alignments of amphipods and to apply the developed methodologies to other systems, thereby assessing the broader applicability of our theories.
From a practical perspective, our study clarifies how beneficial effects of hybridization help species to expand into novel habitats. These processes are relevant for artificial selection, because hybridization is used for breeding new varieties of species in agriculture and biotechnology. We expect that in long perspective our research may be used in biotechnology for estimating positive effects of introgression.
Another important aspect of the research relates to the industrial assessment of water pollution. Amphipods inhabit most freshwater ecosystems worldwide, so various amphipod species serve as bioindicators for water quality testing. We expect that newly sequenced reference genomes will contribute to water quality assessment projects, as no other high-quality genome assemblies of amphipods currently exist.
Finally, our work contributes to the study of a unique and endemic group of species. Species flocks around the world are endangered: African cichlids suffer from overfishing, Lake Baikal amphipods experience water pollution. In a world of constantly shrinking wildlife habitats the importance of studying the diversity we still have left is hard to overestimate.
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