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The lingering problem

As of today the Earth remains the only place known to harbour life. Yet over 99% of species that ever inhabited our planet are estimated to have completely disappeared. This huge loss of life forms reveals the power of natural selection that has, relentlessly, retained the best-adapted creatures over four billion years of history of life. These have gradually evolved in so many ways that trillions of different species have succeeded in colonizing almost all niches available on Earth.

Why has such a puzzling diversity prevailed instead of just a few thousands most successful species? This question drives students of evolution to better understand the causes underlying such an astounding creative process. The KLADOS Fund endeavours to support research projects that advance our knowledge of this fundamental evolution challenge.

The BDM model and internal genetic conflicts

Remarkably, in recent years reproductive isolation by genomic conflict has emerged as a major cause for speciation, with much of the afore mentioned divergence resulting from internal conflicts or responses to mutational mechanisms rather than from ecological adaptation. Genomes are tenuous conglomerates of different genetic entities, each trying to maximize its own evolutionary success, often at great cost to its genomic neighbors, thus resulting in conflicts that can impair the fitness of the host organism. At least in Drosophila, rapidly evolving genes have been shown to be a consequence of such intra-cellular genetic conflicts which include host-parasite interactions and functional incompatibilities, and which underlie the formation of novel species through postzygotic reproductive isolation. Indeed, eukaryotic genomes are constantly challenged by DNA amplification from mobile (transposable) elements as well as by the integration of exogenous viral DNAs or RNAs. When these alterations are detrimental to the fitness of the host, they elicit adaptive compensatory changes in its genome. In order to respond to these iterative challenges, the genome as well as its coevolving compensatory factors can rapidly diverge, which can pave the way to potential hybrid incompatibility. Whenever divergence between physically isolated sub-populations results in functional incompatibilities, these can eventually lead to the formation of two separate species.

Because hybrid incompatibilities are caused by genetic divergence in each of the hybridizing species, they reveal genomic changes with functional consequences occurring on short evolutionary time scales. These changes include divergence in protein-coding gene sequence, structure, and location, as well as divergence in noncoding DNAs such as satellite repeats. With respect to reproductive isolation, recent findings unambiguously point to intra-cellular conflicts involving satellite repeats and chromatin configuration, typically affecting centromere formation and its role in the latest stages of cell division. Satellite repeats make up a large fraction of the genomes of many eukaryotes and are now seen as strong candidates to speciation, being no longer regarded as mere molecular parasites with limited functions. Nonetheless, since closely related species of drosophila have a strongly documented wealth of satellite repeats, comparative studies in this model organism are becoming instrumental in understanding how these rapidly evolving sequences change and move throughout genomes. By and large, satellite repeats have now been found to modulate gene expression and mediate genetic conflicts between chromosomes as well as between sibling species, strongly suggesting that mobile genetic elements together with chromatin configuration play a key role in the speciation process.