Adaptive radiations represent some of the most remarkable explosions of diversification across the tree of life. However, the constraints to rapid diversification and how they are sometimes overcome, particularly the relative roles of genetic architecture and hybridization, remain unclear. Here, we address these questions in the Alpine whitefish radiation, using a whole-genome dataset that includes multiple individuals of each of the 22 species belonging to six ecologically distinct ecomorph classes across several lake-systems. We reveal that repeated ecological and morphological diversification along a common environmental axis is associated with both genome-wide allele frequency shifts and a specific, larger effect, locus, associated with the gene edar. Additionally, we highlight the possible role of introgression between species from different lake-systems in facilitating the evolution and persistence of species with unique trait combinations and ecology. These results highlight the importance of both genome architecture and secondary contact with hybridization in fuelling adaptive radiation.
Ecosystem degradation and biodiversity loss are major global challenges. When reproductive isolation between species is contingent upon the interaction of intrinsic lineage traits with features of the environment, environmental change can weaken reproductive isolation and result in extinction through hybridization. By this process called speciation reversal, extinct species can leave traces in genomes of extant species through introgressive hybridization. Using historical and contemporary samples, we sequenced all four species of an Alpine whitefish radiation before and after anthropogenic lake eutrophication and the associated loss of one species through speciation reversal. Despite the extinction of this taxon, substantial fractions of its genome, including regions shaped by positive selection before eutrophication, persist within surviving species as a consequence of introgressive hybridization during eutrophication. Given the prevalence of environmental change, studying speciation reversal and its genomic consequences provides fundamental insights into evolutionary processes and informs biodiversity conservation.
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Summary Microbes can have profound effects on their hosts, driving natural selection, promoting speciation and determining species distributions. However, soil‐dwelling microbes are rarely investigated as drivers of evolutionary change in plants.We used metabarcoding and experimental manipulation of soil microbiomes to investigate the impact of soil and root microbes in a well‐known case of sympatric speciation, the Howea palms of Lord Howe Island (Australia). Whereas H. forsteriana can grow on both calcareous and volcanic soils, H. belmoreana is restricted to, but more successful on, volcanic soil, indicating a trade‐off in adaptation to the two soil types.We suggest a novel explanation for this trade‐off. Arbuscular mycorrhizal fungi (AMF) are significantly depleted in H. forsteriana on volcanic soil, relative to both H. belmoreana on volcanic soil and H. forsteriana on calcareous soil. This is mirrored by the results of survival experiments, where the sterilization of natural soil reduces Howea fitness in every soil–species combination except H. forsteriana on volcanic soil. Furthermore, AMF‐associated genes exhibit evidence of divergent selection between Howea species.These results show a mechanism by which divergent adaptation can have knock‐on effects on host–microbe interactions, thereby reducing interspecific competition and promoting the coexistence of plant sister species.
Ravinet et al. (2017) focus their review on the genomic landscape of speciation, in particular on the identification of barrier loci. However, here we wish to direct attention towards the evolution of structural rearrangements of the genome. By this, we refer to structural changes in the genome, including deletions, insertions, duplications, inversions and translocations, which alter the genome organization of individuals and result in structural variations within populations and structural differences between species. Within this short comment, we touch on three aspects of this subject, by no means attempting a comprehensive review of the topic. We aim to highlight that genome structure, as well as its sequence, evolves and point out some intrinsic differences between small sequence mutations, including single nucleotides and indels usually smaller than 50 bp, and larger structural variants (SVs) often much larger than 1 kb. The three aspects we judge particularly relevant for considering structural variations in a speciation context and want to review here are (i) the evidence for adaptive SVs, (ii) indications of incompatibilities due to SVs and (iii) the effects of SVs on recombination.
Technological advances in DNA sequencing over the last decade now permit the production and curation of large genomic data sets in an increasing number of nonmodel species. Additionally, these new data provide the opportunity for combining data sets, resulting in larger studies with a broader taxonomic range. Whilst the development of new sequencing platforms has been beneficial, resulting in a higher throughput of data at a lower per‐base cost, shifts in sequencing technology can also pose challenges for those wishing to combine new sequencing data with data sequenced on older platforms. Here, we outline the types of studies where the use of curated data might be beneficial, and highlight potential biases that might be introduced by combining data from different sequencing platforms. As an example of the challenges associated with combining data across sequencing platforms, we focus on the impact of the shift in Illumina's base calling technology from a four‐channel system to a two‐channel system. We caution that when data are combined from these two systems, erroneous guanine base calls that result from the two‐channel chemistry can make their way through a bioinformatic pipeline, eventually leading to inaccurate and potentially misleading conclusions. We also suggest solutions for dealing with such potential artefacts, which make samples sequenced on different sequencing platforms appear more differentiated from one another than they really are. Finally, we stress the importance of archiving tissue samples and the associated sequences for the continued reproducibility and reusability of sequencing data in the face of ever‐changing sequencing platform technology.
Supergenes maintain adaptive clusters of alleles in the face of genetic mixing. Although usually attributed to inversions, supergenes can be complex, and reconstructing the precise processes that led to recombination suppression and their timing is challenging. We investigated the origin of the BC supergene, which controls variation in warning coloration in the African monarch butterfly, Danaus chrysippus . By generating chromosome-scale assemblies for all three alleles, we identified multiple structural differences. Most strikingly, we find that a region of more than 1 million bp underwent several segmental duplications at least 7.5 Ma. The resulting duplicated fragments appear to have triggered four inversions in surrounding parts of the chromosome, resulting in stepwise growth of the region of suppressed recombination. Phylogenies for the inversions are incongruent with the species tree and suggest that structural polymorphisms have persisted for at least 4.1 Myr. In addition to the role of duplications in triggering inversions, our results suggest a previously undescribed mechanism of recombination suppression through independent losses of divergent duplicated tracts. Overall, our findings add support for a stepwise model of supergene evolution involving a variety of structural changes. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.
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