The evolution of the genomic landscape in Silvereyes does not follow theoretical predictions

The accumulation of genetic differences is unrelated to the development of genomic islands.

Imagine going for a walk through a mountainous region. You work your way up steep slopes, venture into valleys and stroll across expansive plateaus. You don’t even have to go outdoors to explore such heterogenous landscapes, just sequence a few genomes and compare the level of genetic differentiation of two species along these seemingly endless stretches of A, T, C and Gs. Indeed, numerous studies have described a heterogenous genomic landscape with highly divergent mountains and undifferentiated valleys. I have made my modest contribution to this field of research by exploring the genomic landscape of two goose taxa (you can read the whole story here).

The mechanisms responsible for these heterogenous genomic landscapes are still a matter of debate. The most often invoked verbal model goes as follows. At the onset of speciation, genetic differentiation is restricted to a few genomic regions that are under strong selection, resulting in peaks of divergence (the so-called “genomic islands”). As the speciation process continues and the diverging populations go their separate evolutionary ways, these genomic islands are predicted to expand through the linkage with neutral and weakly selected loci. This process – known as genetic hitchhiking – can be influenced by gene flow. The exchange of DNA between the diverging populations can homogenize certain genomic regions and slow down the expansion of genomic islands.

Testing Predictions

These theoretical predictions make intuitive sense but remains to be tested in different study systems. One possible approach is to compare diverging populations at different stages of the speciation process. A recent study in the journal G3: Genes|Genomes|Genetics applied this approach to the Silvereye (Zosterops lateralis), comparing population pairs that varied in their divergence timeframes (early stage:,150 years, mid stage: 3,000-4,000 years, and late stage: 100,000s years) and their mode of divergence (with gene flow or without gene flow).

In contrast to the predictions outlines above, the researchers did not find support for the genetic hitchhiking model. They write that “Genomic islands were rarely associated with SNPs putatively under selection and genomic islands did not widen as expected under the divergence hitchhiking model of speciation.” It seemed that the build-up of genetic divergence mostly occurred outside genomic islands. In addition, simulations suggested that the transition from localized divergence to genome-wide divergence can proceed without selection. All in all, these results question the theoretical model of genetic hitchhiking.

In contrast to the predictions of the genetic hitchhiking model, the genomic islands of differentiation did not expand with increasing divergence times. From: Sendell-Price et al. (2020) G3: Genes|Genomes|Genetics.

Theory and Practice

The authors concluded that “Genome-wide divergence in silvereyes does not hinge on the formation and growth of genomic islands.” Does this mean that we should discard the genetic hitchhiking model of speciation? Not necessarily, because the current study focused on recently diverged populations (with a late stage of ca. 100,000 years). Perhaps genetic hitchhiking becomes more apparent at larger times scales, such as millions of years. Comparisons between more diverged Zosterops species are needed to confirm this.

This study nicely illustrates the interplay between theory and practice. The genetic hitchhiking model is based on solid, theoretical thinking and provides several testable predictions (as a good model should). Results that are not in line with these predictions will help to improve the theoretical model (or discard it if too many incongruent observations start piling up). Hence, with rigorous analyses and the fine-tuning of our thinking, we slowly expand our knowledge on the genomic mechanisms underlying the origin of new species. This quote from Yogi Berra seems like fitting end to this blog post: “In theory there is no difference between theory and practice. In practice there is.”

References

Sendell-Price, A. T., Ruegg, K. C., Anderson, E. C., Quilodrán, C. S., Van Doren, B. M., Underwood, V. L., Coulson, T. & Clegg, S. M. (2020). The genomic landscape of divergence across the speciation continuum in island-colonising silvereyes (Zosterops lateralis). G3: Genes|Genomes|Genetics10(9), 3147-3163.

Featured image: Silvereye (Zosterops lateralis) © Bernard Spragg | Wikimedia Commons

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