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Many Drosophila species differ widely in their distributions and climate niches, making them excellent subjects for evolutionary genomic studies. Here, we have developed a database of high-quality assemblies for 46 Drosophila species and one closely related Zaprionus. Fifteen of the genomes were newly sequenced, and 20 were improved with additional sequencing. New or improved annotations were generated for all 47 species, assisted by new transcriptomes for 19. Phylogenomic analyses of these data resolved several previously ambiguous relationships, especially in the melanogaster species group. However, it also revealed significant phylogenetic incongruence among genes, mainly in the form of incomplete lineage sorting in the subgenus Sophophora but also including asymmetric introgression in the subgenus Drosophila. Using the phylogeny as a framework and taking into account these incongruences, we then screened the data for genome-wide signals of adaptation to different climatic niches. First, phylostratigraphy revealed relatively high rates of recent novel gene gain in three temperate pseudoobscura and five desert-adapted cactophilic mulleri subgroup species. Second, we found differing ratios of nonsynonymous to synonymous substitutions in several hundred orthologues between climate generalists and specialists, with trends for significantly higher ratios for those in tropical and lower ratios for those in temperate-continental specialists respectively than those in the climate generalists. Finally, resequencing natural populations of 13 species revealed tropics-restricted species generally had smaller population sizes, lower genome diversity and more deleterious mutations than the more widespread species. We conclude that adaptation to different climates in the genus Drosophila has been associated with large-scale and multifaceted genomic changes.

When closely related species come into contact via range expansion, both may experience reduced fitness as a result of the interaction. Selection is expected to favour traits that minimize costly interspecies reproductive interactions (such as mismating) via a phenomenon called reproductive character displacement (RCD). Research on RCD frequently assumes secondary contact between species, but the geographical history of species interactions is often unknown. Population genomic data permit tests of geographical hypotheses about species origins and secondary contact through range expansion. We used population genomic data from single nucleotide polymorphisms (SNPs), mitochondrial sequence data, advertisement call data and morphological data to investigate a species complex of toadlets (Uperoleia borealis, U. crassa, U. inundata) from northern Australia. Although the three species of frogs were morphologically indistinguishable in our analysis, we determined that U. crassa and U. inundata form a single species (synonymized here) based on an absence of genomic divergence. SNP data identified the phylogeographical origin of U. crassa as the Top End, with subsequent westward invasion into the range of U. borealis in the Kimberley. We identified six F1 hybrids, all of which had the U. borealis mitochondrial haplotype, suggesting unidirectional hybridization. Consistent with the RCD hypothesis, U. borealis and U. crassa sexual signals differ more in sympatry than in allopatry. Hybrid males have intermediate calls, which probably reduces attractiveness to females. Integrating population genomic data, mitochondrial sequencing, morphology and behavioural approaches provides an unusually detailed collection of evidence for reproductive character displacement following range expansion and secondary contact.

When closely related species come into contact via range expansion, both may experience reduced fitness as a result of the interaction. Selection is expected to favour traits that minimize costly interspecies reproductive interactions (such as mismating) via a phenomenon called reproductive character displacement (RCD). Research on RCD frequently assumes secondary contact between species, but the geographical history of species interactions is often unknown. Population genomic data permit tests of geographical hypotheses about species origins and secondary contact through range expansion. We used population genomic data from single nucleotide polymorphisms (SNPs), mitochondrial sequence data, advertisement call data and morphological data to investigate a species complex of toadlets (Uperoleia borealis, U. crassa, U. inundata) from northern Australia. Although the three species of frogs were morphologically indistinguishable in our analysis, we determined that U. crassa and U. inundata form a single species (synonymized here) based on an absence of genomic divergence. SNP data identified the phylogeographical origin of U. crassa as the Top End, with subsequent westward invasion into the range of U. borealis in the Kimberley. We identified six F1 hybrids, all of which had the U. borealis mitochondrial haplotype, suggesting unidirectional hybridization. Consistent with the RCD hypothesis, U. borealis and U. crassa sexual signals differ more in sympatry than in allopatry. Hybrid males have intermediate calls, which probably reduces attractiveness to females. Integrating population genomic data, mitochondrial sequencing, morphology and behavioural approaches provides an unusually detailed collection of evidence for reproductive character displacement following range expansion and secondary contact.

When closely related species come into contact via range expansion, both may experience reduced fitness as a result of the interaction. Selection is expected to favour traits that minimize costly interspecies reproductive interactions (such as mismating) via a phenomenon called reproductive character displacement (RCD). Research on RCD frequently assumes secondary contact between species, but the geographical history of species interactions is often unknown. Population genomic data permit tests of geographical hypotheses about species origins and secondary contact through range expansion. We used population genomic data from single nucleotide polymorphisms (SNPs), mitochondrial sequence data, advertisement call data and morphological data to investigate a species complex of toadlets (Uperoleia borealis, U. crassa, U. inundata) from northern Australia. Although the three species of frogs were morphologically indistinguishable in our analysis, we determined that U. crassa and U. inundata form a single species (synonymized here) based on an absence of genomic divergence. SNP data identified the phylogeographical origin of U. crassa as the Top End, with subsequent westward invasion into the range of U. borealis in the Kimberley. We identified six F1 hybrids, all of which had the U. borealis mitochondrial haplotype, suggesting unidirectional hybridization. Consistent with the RCD hypothesis, U. borealis and U. crassa sexual signals differ more in sympatry than in allopatry. Hybrid males have intermediate calls, which probably reduces attractiveness to females. Integrating population genomic data, mitochondrial sequencing, morphology and behavioural approaches provides an unusually detailed collection of evidence for reproductive character displacement following range expansion and secondary contact.

When closely related species come into contact via range expansion, both may experience reduced fitness as a result of the interaction. Selection is expected to favour traits that minimize costly interspecies reproductive interactions (such as mismating) via a phenomenon called reproductive character displacement (RCD). Research on RCD frequently assumes secondary contact between species, but the geographical history of species interactions is often unknown. Population genomic data permit tests of geographical hypotheses about species origins and secondary contact through range expansion. We used population genomic data from single nucleotide polymorphisms (SNPs), mitochondrial sequence data, advertisement call data and morphological data to investigate a species complex of toadlets (Uperoleia borealis, U. crassa, U. inundata) from northern Australia. Although the three species of frogs were morphologically indistinguishable in our analysis, we determined that U. crassa and U. inundata form a single species (synonymized here) based on an absence of genomic divergence. SNP data identified the phylogeographical origin of U. crassa as the Top End, with subsequent westward invasion into the range of U. borealis in the Kimberley. We identified six F1 hybrids, all of which had the U. borealis mitochondrial haplotype, suggesting unidirectional hybridization. Consistent with the RCD hypothesis, U. borealis and U. crassa sexual signals differ more in sympatry than in allopatry. Hybrid males have intermediate calls, which probably reduces attractiveness to females. Integrating population genomic data, mitochondrial sequencing, morphology and behavioural approaches provides an unusually detailed collection of evidence for reproductive character displacement following range expansion and secondary contact.