Abstract
The repeatability or predictability of evolution is a central question in evolutionary biology and most often addressed in experimental evolution studies. Here, we infer how genetically heterogeneous natural systems acquire the same molecular changes to address how genomic background affects adaptation in natural populations. In particular, we take advantage of independently formed neo-sex chromosomes in Drosophila species that have evolved dosage compensation by co-opting the dosage-compensation male-specific lethal (MSL) complex to study the mutational paths that have led to the acquisition of hundreds of novel binding sites for the MSL complex in different species. This complex recognizes a conserved 21-bp GA-rich sequence motif that is enriched on the X chromosome, and newly formed X chromosomes recruit the MSL complex by de novo acquisition of this binding motif. We identify recently formed sex chromosomes in the D. melanica and D. robusta species groups by genome sequencing and generate genomic occupancy maps of the MSL complex to infer the location of novel binding sites. We find that diverse mutational paths were utilized in each species to evolve hundreds of de novo binding motifs along the neo-X, including expansions of microsatellites and transposable element (TE) insertions. However, the propensity to utilize a particular mutational path differs between independently formed X chromosomes and appears to be contingent on genomic properties of that species, such as simple repeat or TE density. This establishes the “genomic environment” as an important determinant in predicting the outcome of evolutionary adaptations.
Highlights
What would happen if we “replay the tape of life” [1]? The question of whether adaptation follows a deterministic route largely prescribed by the environment or whether evolution is fundamentally unpredictable and can proceed along a large number of alternative trajectories has until recently been a fascinating problem that could not be addressed directly.In the past decade, advances in DNA sequencing technology have allowed researchers to tackle this question using two complementary approaches
We address how predictable evolution is at the DNA sequence level in nature by studying the parallel evolution of a phenotype that is well understood at the molecular level: the acquisition of sex chromosome dosage compensation in fruit flies
We recently studied the evolution of male-specific lethal (MSL)-binding sites in D. miranda, a model species for sex chromosome evolution that possesses two neo-X chromosomes that were formed about 13–15 million years (MY) and 1.5 MY ago, respectively [19,20]
Summary
What would happen if we “replay the tape of life” [1]? The question of whether adaptation follows a deterministic route largely prescribed by the environment or whether evolution is fundamentally unpredictable and can proceed along a large number of alternative trajectories has until recently been a fascinating problem that could not be addressed directly.In the past decade, advances in DNA sequencing technology have allowed researchers to tackle this question using two complementary approaches. Genomic analysis of populations experimentally evolved under controlled laboratory conditions has consistently revealed parallelism in which mutations in certain genes are repeatedly selected [3,4]. These studies are typically limited to systems that can be rapidly propagated in the lab and many relevant evolutionary parameters (such as environment, population size, etc.) are controlled by the experiment, and their applicability to natural systems is sometimes unclear [5]. The parameters of convergent evolution in protein-coding genes are fairly well understood and often involve a small number of amino-acid mutations of large effect size that are constrained to specific regions of the protein because of pleiotropy. Convergent regulatory evolution involves a much larger set of mutational targets and mechanisms: A
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