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Reconstructing the evolution of baleen whales (Mysticeti) has been problematic because morphological and genetic analyses have produced different scenarios. This might be caused by genomic admixture that may have taken place among some rorquals. We present the genomes of six whales, including the blue whale (Balaenoptera musculus), to reconstruct a species tree of baleen whales and to identify phylogenetic conflicts. Evolutionary multilocus analyses of 34,192 genome fragments reveal a fast radiation of rorquals at 10.5 to 7.5 million years ago coinciding with oceanic circulation shifts. The evolutionarily enigmatic gray whale (Eschrichtius robustus) is placed among rorquals, and the blue whale genome shows a high degree of heterozygosity. The nearly equal frequency of conflicting gene trees suggests that speciation of rorqual evolution occurred under gene flow, which is best depicted by evolutionary networks. Especially in marine environments, sympatric speciation might be common; our results raise questions about how genetic divergence can be established.
The iconic Australasian kangaroos and wallabies represent a successful marsupial radiation. However, the evolutionary relationship within the two genera, Macropus and Wallabia, is controversial: mitochondrial and nuclear genes, and morphological data have produced conflicting scenarios regarding the phylogenetic relationships, which in turn impact the classification and taxonomy. We sequenced and analyzed the genomes of 11 kangaroos to investigate the evolutionary cause of the observed phylogenetic conflict. A multilocus coalescent analysis using ∼14,900 genome fragments, each 10 kb long, significantly resolved the species relationships between and among the sister-genera Macropus and Wallabia. The phylogenomic approach reconstructed the swamp wallaby (Wallabia) as nested inside Macropus, making this genus paraphyletic. However, the phylogenomic analyses indicate multiple conflicting phylogenetic signals in the swamp wallaby genome. This is interpreted as at least one introgression event between the ancestor of the genus Wallabia and a now extinct ghost lineage outside the genus Macropus. Additional phylogenetic signals must therefore be caused by incomplete lineage sorting and/or introgression, but available statistical methods cannot convincingly disentangle the two processes. In addition, the relationships inside the Macropus subgenus M. (Notamacropus) represent a hard polytomy. Thus, the relationships between tammar, red-necked, agile, and parma wallabies remain unresolvable even with whole-genome data. Even if most methods resolve bifurcating trees from genomic data, hard polytomies, incomplete lineage sorting, and introgression complicate the interpretation of the phylogeny and thus taxonomy.
Retrophylogenomics in rorquals indicate large ancestral population sizes and a rapid radiation
(2019)
Background: Baleen whales (Mysticeti) are the largest animals on earth and their evolutionary history has been studied in detail, but some relationships still remain contentious. In particular, reconstructing the phylogenetic position of the gray whales (Eschrichtiidae) has been complicated by evolutionary processes such as gene flow and incomplete lineage sorting (ILS). Here, whole-genome sequencing data of the extant baleen whale radiation allowed us to identify transposable element (TE) insertions in order to perform phylogenomic analyses and measure germline insertion rates of TEs. Baleen whales exhibit the slowest nucleotide substitution rate among mammals, hence we additionally examined the evolutionary insertion rates of TE insertions across the genomes.
Results: In eleven whole-genome sequences representing the extant radiation of baleen whales, we identified 91,859 CHR-SINE insertions that were used to reconstruct the phylogeny with different approaches as well as perform evolutionary network analyses and a quantification of conflicting phylogenetic signals. Our results indicate that the radiation of rorquals and gray whales might not be bifurcating. The morphologically derived gray whales are placed inside the rorqual group, as the sister-species to humpback and fin whales. Detailed investigation of TE insertion rates confirm that a mutational slow down in the whale lineage is present but less pronounced for TEs than for nucleotide substitutions.
Conclusions: Whole genome sequencing based detection of TE insertions showed that the speciation processes in baleen whales represent a rapid radiation. Large genome-scale TE data sets in addition allow to understand retrotransposition rates in non-model organisms and show the potential for TE calling methods to study the evolutionary history of species.