Chromosome-Level Genome Assembly of Eden's Whale Clarifies the Taxonomy and Speciation of Bryde's Whale Complex

Abstract

Eden's whale (Balaenoptera edeni), a poorly understood baleen cetacean, has long been shrouded in taxonomic ambiguity due to limited genomic resources, obscuring its distinction from closely related species and its position within the cetacean Tree of Life. In this paper, we present a high-quality chromosomal-level genome of B. edeni and conduct comparative genomic analyses to address long-standing taxonomic confusion and elucidate speciation of balaenopterids. Our phylogenomic analysis and demographic reconstruction reveal that B. edeni is a distinct sister to Bryde's whale (Balaenoptera brydei), sharing a common ancestor that diverged approximately 7.84 million years ago during the late Miocene. Their genetic divergence exceeds typical intraspecific variation in whales, supporting the reinstatement of B. brydei as a valid species. Chromosomal syntenic analyses suggest that macro-fragment inversions contributed to speciation in balaenopterid whales and uncover unexpected large-scale complex genome rearrangements in Bryde's whale, offering novel insights into cetacean genome evolution. Functional enrichment analysis of inverted regions between B. edeni and Balaenoptera musculus indicates their predominant association with metabolism and biosynthesis, as well as responses to various substances, stress, and stimuli. These genomic resources for B. edeni not only lay a critical foundation for comparative genetic and evolutionary research of cetaceans but also advance our understanding of the taxonomy and evolutionary dynamics of the Bryde's whale complex, with broader implications for baleen whale conservation and biodiversity.

Keywords: Balaenoptera; Mysticeti; cetacean; evolution; marine mammal.

Fig. 1.

Genomic structure and phylogenomic relationships of Eden's whale. a) Circus plot of 23 linkage groups (corresponding to chromosomes) showing marker distributions at 1 Mb sliding windows from outer to inner circle: gene density, GC content, and GC skew. The animal icon in the center of the circus plot was obtained from the Plazi's databases (https://plazi.org/) without copyright restriction. b) Structure of the mitogenome showing protein-coding genes and RNAs. c) Phylogenomic relationships, divergent times, and expanded and contracted gene families of cetaceans with hippo as the outgroup. The tree was constructed using 3,360 single-copy orthogroups. The bootstrap values are 100 at all nodes. The tree was fossil-calibrated at five nodes. The bar length indicated the 95% confidence interval. Sources and characteristics of the genomes are included in Table S2. The bar plot shows the number of significantly expanded and contracted gene families in each species relative to its nearest node, with a P-value < 0.05. The animal icons do not represent their real body sizes. They were obtained from the Phylopic website (https://www.phylopic.org/) without copyright restriction. d) The best putative divergence scenario of Bryde's whale complex (Scenario 1) based on the randomly sampled SNP dataset (N = 10,295). Other scenarios are shown in Fig. S3. N1, Balaenoptera ricei (BRic); N2, B. brydei (BBry); N3, B. edeni (BEde); N3b, putative mimics demographic bottleneck; t2, time point of first divergence event from the ancestor; from t2 to 0, from the ancient to present.

Fig. 2.

Synteny relationship between Eden's whale and its relatives. a) Ribbon diagram showing the microsynteny between the chromosomes of Eden's whale and its relatives. b) Macrosynteny between Eden's, blue, and Bryde's whales, and the hippo. c) Inter-chromosomal synteny between Eden's and Bryde's whales. d) Chromosomal rearrangement index of selected genomes references Eden's whale and hippo, respectively. The animal icons were obtained from the Plazi's databases (https://plazi.org/) without copyright restriction.

Fig. 3.

Specific chromosome structures and variations between Eden's and blue whales. a) Inversion macro-fragments in four chromosomes of Eden's whale compared to those of the blue whale. b) Top 30% GO functional enrichment, based on genes within the four inversion macrofragments of Eden's whale, showing their main functions of metabolism, biosynthesis, and responses. c) Gene synteny of the Y chromosomes of Eden's and blue whales.