doi: 10.1126/sciadv.aap9873. eCollection 2018 Apr.
Whole-genome sequencing of the blue whale and other rorquals finds signatures for introgressive gene flow
Affiliations
- PMID:29632892
- PMCID: PMC5884691
- DOI: 10.1126/sciadv.aap9873
Item in Clipboard
Whole-genome sequencing of the blue whale and other rorquals finds signatures for introgressive gene flow
Úlfur Árnason et al. Sci Adv..
Display options
Format
Display options
Format
Abstract
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.
Figures
(A) An MSC species tree was constructed from 34,192 individual GFs. Internal branches within Balaenopteridae are numbered 1 to 7. All branches receive maximal support (P = 1.0, ASTRAL analysis). Branch lengths were calculated from an ML analysis. Gray whales, family Eschrichtiidae, are placed inside Balaenopteridae as a sister group to fin and humpback whales. (B) ASTRAL quartet-score analyses for branches 1 to 7 (A). Quartet scores were calculated for the three possible arrangements (q1 to q3) for the respective branch. The principal quartet trees are depicted, with q1 representing the species tree. Branch nos. 2 and 3 receive only limited quartet scores, and no quartet can be significantly rejected.
Conflicting evolutionary signals characterize the center of the network, which is equivalent to branch no. 3 in the species tree (Fig. 1). In addition, placing the minke whale has some conflicting signal, but the elongated rectangle indicates a higher degree of resolution. The number of supporting GFs is shown for selected splits. Colored circles indicate taxonomic classification. Blue,Balaenoptera; red,Megaptera; yellow,Eschrichtius; green,Balaena andEubalaena.
(A) The species tree of baleen whales with gene flow signals detected by theD statistic andDFOIL indicated by dashed lines. Signals I to IV were inferred by theD statistic, and signals V, VI, and VII were detected byDFOIL and were partially corroborated by theD statistic. Note thatDFOIL cannot infer gene flow involving the minke whale. (B toD) Rooted networks for the Balaenopteridae sensu lato phylogeny with reticulations inferred from PhyloNet based on 34,192 20-kbp GFs. Reticulations are shown as blue arrows with inheritance probability denoted above or below. Log-likelihood scores are shown below the networks. Notably, inheritance probability around 33% resembles the distribution of quartet scores and the phylogenetic signals from GFs (Fig. 1). (B) The three best networks indicated a reticulation originating at the circled three branches to minke whale. Similar likelihood scores do not allow the identification of a single origin of gene flow; therefore, the networks were merged, and a range of inheritance probabilities is given. (C) The fourth best network has only a marginally poorer likelihood score and indicates a reticulation between the ancestor of the fin and humpback whale and that of the minke whale. (D) The fifth best network has the same likelihood as (C) and finds an alternative placement of gray whale (blue branch) and reticulation from the ancestor of the blue and sei whale to that of the minke whale.
(A) Genome-wide heterozygosity estimated from genomic 100-kbp windows. (B) HistoricalNe using the PSMC analyses for all baleen whale genomes. Thex axis shows the time, and they axis showsNe. Plots were scaled using a mutation rate (μ) of 1.39 × 10−8 substitutions nucleotide−1 generation−1 and species-specific generation times (g). Generation times are noted next to the species names. Light brown shading indicates interglacials (IG) in the Pleistocene and Holocene, and gray shading indicates the MPT and the PPT.
Rorquals diverged in the late Miocene, 10.5 to 7.5 Ma ago. Four other cetartiodactyl species were also included but not shown due to space constraints; the dog (Canis lupus familiaris) was used as an outgroup. Five calibration points were used for dating (table S8) (, –60).
References
- R. M. Nowak,Walker’s Mammals of the World (Johns Hopkins Univ. Press, ed. 6, 1999).
- A. Werth, inFeeding: Form, Function, and Evolution in Tetrapod Vertebrates, K. Schwenk, Ed. (Academic Press, 2000), pp. 487–526.
- Hassanin A., Delsuc F., Ropiquet A., Hammer C., Jansen van Vuuren B., Matthee C., Ruiz-Garcia M., Catzeflis F., Areskoug V., Nguyen T. T., Couloux A., Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C. R. Biol. 335, 32–50 (2012). - PubMed
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Other Literature Sources