Tuesday, November 30, 2021

[Ichthyology • 2021] Speciation Dynamics and Extent of Parallel Evolution along A Lake-Stream Environmental Contrast in African Cichlid Fishes


Astatotilapia burtoni, Haplochromis stappersii,
Ctenochromis horei, 
and Pseudocrenilabrus philander

in Weber, Rajkov, ... et Salzburger, 2021 
Artwork by    twitter.com/jehimes

Abstract
Understanding the dynamics of speciation is a central topic in evolutionary biology. Here, we investigated how morphological and genomic differentiation accumulated along the speciation continuum in the African cichlid fish Astatotilapia burtoni. While morphological differentiation was continuously distributed across different lake-stream population pairs, we found that there were two categories with respect to genomic differentiation, suggesting a “gray zone” of speciation at ~0.1% net nucleotide divergence. Genomic differentiation was increased in the presence of divergent selection and drift compared to drift alone. The quantification of phenotypic and genetic parallelism in four cichlid species occurring along a lake-stream environmental contrast revealed parallel and antiparallel components in rapid adaptive divergence, and morphological convergence in species replicates inhabiting the same environments. Furthermore, we show that the extent of parallelism was higher when ancestral populations were more similar. Our study highlights the complementary roles of divergent selection and drift on speciation and parallel evolution.

The study system comprising nine lake-stream population pairs in four cichlid fish species from African Lake Tanganyika and surroundings.
(A) Illustrations of the four species used in this study and a schematic representation of their phylogenetic relationships.
(B) Map of sampling localities and names of the different lake-stream population pairs, that is, systems. Astatotilapia burtoni, Ctenochromis horei, Haplochromis stappersii, and Pseudocrenilabrus philander.

    

CONCLUSION: 
By examining the dynamics of differentiation in the African cichlid A. burtoni, we found that morphological differentiation was continuous along the speciation continuum. Contrastingly, we detected a gap in genomic differentiation that was only partially explained by geographic patterns. Our results, therefore, provide additional support for the hypothesis that there is a tipping point in genomic differentiation during the speciation process (5), suggesting that there might be a threshold of genomic differentiation to delimit species. We further showed that genomic differentiation was accelerated in the presence of both divergent selection and genetic drift, highlighting the combined effect of selective and neutral processes in speciation.
To gain insights into the potential predictability of the speciation process, we investigated the extent of parallel evolution in nine population pairs from four cichlid species that diverged along a similar lake-stream environmental contrast. While pairwise comparisons failed to identify strong signatures of phenotypic and genomic parallelism, multivariate analyses uncovered major axes of shared evolutionary changes along the lake-stream contrast. Last, we found that levels of parallelism were higher between closely related and, hence, genetically more similar population pairs. While the speciation process is overall difficult to predict, our results support the view that evolution can be predictable to a certain extent if appropriate models and data are used (56). To conclude, our study corroborates that contingency plays an important role in speciation and that speciation is a complex product of differentiation trajectories through multivariate space and time.



Alexandra A.-T. Weber, Jelena Rajkov, Kolja Smailus, Bernd Egger and Walter Salzburger. 2021 Speciation Dynamics and Extent of Parallel Evolution along A Lake-Stream Environmental Contrast in African Cichlid Fishes. SCIENCE ADVANCES. 7: 45. DOI: 10.1126/sciadv.abg5391