Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers.
Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d(xy) and relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Reto
R
Burri
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Alexander
A
Nater
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Takeshi
T
Kawakami
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Carina F
CF
Mugal
Wallenberg Advanced Bioinformatics Infrastructure (WABI), Science for Life Laboratory, Uppsala University, 75123 Uppsala, Sweden;
Pall I
PI
Olason
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Linnea
L
Smeds
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Alexander
A
Suh
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Ludovic
L
Dutoit
Laboratory of Ornithology, Department of Zoology, Palacky University, 77146 Olomouc, Czech Republic;
Stanislav
S
Bureš
Department of Evolutionary Ecology, Estación Biológica de Doñana-CSIC, 41092 Seville, Spain;
Laszlo Z
LZ
Garamszegi
Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, 0316 Oslo, Norway; Natural History Museum, University of Oslo, 0318 Oslo, Norway;
Silje
S
Hogner
Museo Nacional de Ciencias Naturales-CSIC, 28006 Madrid, Spain;
Juan
J
Moreno
Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Anna
A
Qvarnström
Bird Protection and Study Society of Serbia, Radnička 20a, 21000 Novi Sad, Serbia;
Milan
M
Ružić
Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, 0316 Oslo, Norway; Norwegian Institute for Nature Research (NINA), 7034 Trondheim, Norway;
Stein-Are
SA
Sæther
Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, 0316 Oslo, Norway;
Glenn-Peter
GP
Sætre
Behavioural Ecology Group, Department of Systematic Zoology and Ecology, Eötvös Loránd University, 1117 Budapest, Hungary.
Janos
J
Török
Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, 75236 Uppsala, Sweden;
Hans
H
Ellegren
D000818:Animals; D005260:Female; D051456:Gene Flow; D049810:Genetic Speciation; D005828:Genetics, Population; D016678:Genome; D023281:Genomics; D060005:Genotyping Techniques; D008297:Male; D046109:Passeriformes / Q000145:classification* / Q000235:genetics*; D020641:Polymorphism, Single Nucleotide; D011995:Recombination, Genetic; D060047:Reproductive Isolation; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA; D013045:Species Specificity