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. 2020 Oct 3;23(10):101640. doi: 10.1016/j.isci.2020.101640

An Indo-Pacific Humpback Dolphin Genome Reveals Insights into Chromosome Evolution and the Demography of a Vulnerable Species

Peijun Zhang 1,4,23, Yong Zhao 2,23, Chang Li 2,8,23, Mingli Lin 1, Lijun Dong 1, Rui Zhang 2, Mingzhong Liu 1, Kuan Li 1, He Zhang 2,20, Xiaochuan Liu 2, Yaolei Zhang 2,21, Yuan Yuan 1,11, Huan Liu 3, Inge Seim 9,10, Shuai Sun 2, Xiao Du 2, Yue Chang 2, Feida Li 3, Shanshan Liu 2, Simon Ming-Yuen Lee 5, Kun Wang 11, Ding Wang 12, Xianyan Wang 13, Michael R McGowen 14, Thomas A Jefferson 15, Morten Tange Olsen 16, Josefin Stiller 4, Guojie Zhang 4,6,19, Xun Xu 2,3, Huanming Yang 3,6, Guangyi Fan 2,5,∗, Xin Liu 2,3,7,18,∗∗, Songhai Li 1,17,22,24,∗∗∗
PMCID: PMC7569330  PMID: 33103078

Summary

The Indo-Pacific humpback dolphin (Sousa chinensis) is a small inshore species of odontocete cetacean listed as Vulnerable on the IUCN Red List. Here, we report on the evolution of S. chinensis chromosomes from its cetruminant ancestor and elucidate the evolutionary history and population genetics of two neighboring S. chinensis populations. We found that breakpoints in ancestral chromosomes leading to S. chinensis could have affected the function of genes related to kidney filtration, body development, and immunity. Resequencing of individuals from two neighboring populations in the northwestern South China Sea, Leizhou Bay and Sanniang Bay, revealed genetic differentiation, low diversity, and small contemporary effective population sizes. Demographic analyses showed a marked decrease in the population size of the two investigated populations over the last ~4,000 years, possibly related to climatic oscillations. This study implies a high risk of extinction and strong conservation requirement for the Indo-Pacific humpback dolphin.

Subject Areas: Evolutionary Biology, Genetics, Genomics

Graphical Abstract

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Highlights

  • •

    Deducing chromosome evolution from ancestral Cetruminantia and ancestral Odontoceti

  • •

    Reconstructing the demographic history of Sousa chinensis

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    Implying high risk of extinction and strong conservation requirement for S. chinensis

Evolutionary Biology; Genetics; Genomics

Introduction

A fascinating example of evolution is the return of terrestrial mammals to an aquatic environment. This occurred at least three separate times independently and is manifested by functional adaptations in 129 extant species in three major marine mammal lineages: Cetacea (whales, dolphins, and porpoises), Pinnipedia (walruses, sea lions, and seals), and Sirenia (manatees and dugongs) (Committee on Taxonomy, 2020). Recent genome-scale analyses of marine mammals have provided unprecedented insights into their evolution, adaptations, and demographic histories, highlighting the urgent need for conservation and management of many species (Árnason et al., 2018; Autenrieth et al., 2018; Brüniche-Olsen et al., 2018; Foote et al., 2015; Jones et al., 2017; Keane et al., 2015; Moskalev et al., 2017; Warren et al., 2017; Yim et al., 2014; Zhou et al., 2018a; Zhou et al., 2015; Zhou et al., 2018b; Zhou et al., 2013). Despite these advances, the genome of most marine mammals has yet to be sequenced, and cetacean genome assemblies published to date are often highly fragmented (e.g., see Zhou et al., 2018a), leaving research questions related to genomic structural evolution unanswered. A chromosome-level genome is fundamental for many downstream studies, including the analysis on whole-genome duplications (WGDs) and chromosome rearrangement events (Eichler and Sankoff, 2003). WGDs have been reported to strongly impact genome evolution and species formation in vertebrates. For example, all ray-finned fishes (Actinopterygia), accounting for 99% of teleosts, are shaped by a third WGD events (Van de Peer et al., 2009). Chromosome rearrangement usually accompanies the gain/loss of entire genes or regulatory regions, and is believed to play important roles in the evolution of lineage-specific traits and even speciation (Kirkpatrick, 2010). Thus, chromosome-level reference genomes are key for evolutionary analyses and conservation efforts of cetaceans (Moura et al., 2014; Viricel et al., 2014).

The Indo-Pacific humpback dolphin (Sousa chinensis; known as the Chinese white dolphin in China) is a small, toothed whale (Odontoceti) that occupies shallow tropical to temperate coastal habitats, from the Bay of Bengal to central China and throughout Southeast Asia (Jefferson and Rosenbaum, 2014; Jefferson and Smith, 2016). In recent decades, S. chinensis populations have been reported to face threats including by-catch in nets and overfishing (Dans et al., 2003), water pollution (Liu et al., 2018a), heavy marine traffic (Ng and Leung, 2003), and coastal development (Jefferson et al., 2009). Consequently, S. chinensis populations are declining (Huang et al., 2012), and the species is considered Vulnerable to extinction by the International Union for Conservation of Nature (Jefferson and Smith, 2016; Li, 2020). S. chinensis has also been listed as a Grade 1 National Key Protected Animal since 1988 in China, a distinction shared with the Yangtze River dolphin (baiji; Lipotes vexillifer), which was declared functionally extinct in 2007 (Turvey et al., 2007). The management and conservation of this Vulnerable species could be improved by a better understanding of its evolutionary history, inshore adaption, and population dynamics. Here, we traced both genomic reshuffling events and obtained population-level genetic data to illustrate how S. chinensis evolved in shallow tropical to temperate coastal habitats and predict its likely future population dynamics.

Results

We generated ~317 Gb (129×) of S. chinensis genome data, using 10X Genomics technology (Pleasanton, CA, USA) on the BGISEQ-500 sequencing platform (Table S1) and assembled a 2.46-Gb draft genome sequence with a contig N50 of 114 kb and a scaffold N50 of 27.7 Mb, respectively (Table S2). To assign the draft genome assembly onto chromosomes, we produced ~73-Gb Hi-C data (Figures S1–S4) and anchored ~90.7% of genome scaffolds into 22 chromosomes (Figure S5 and Table S3). Overall, contig and scaffold metrics of this genome is higher than recently reported S. chinensis assemblies that were not resolved at the chromosome level (Jia et al., 2019; Ming et al., 2019) (Table S4). We annotated 20,767 protein-coding genes (Figure S6). Assessment with BUSCO (mammalia_odb9 gene set) revealed a high proportion of complete gene models in the genome assembly (~91.9%) and a reliable protein-coding gene set (~97.3%) (Table S5). We identified 17,286 gene families in S. chinensis by clustering genes with eight other mammals (human, sheep, cattle, finless porpoise, horse, minke whale, bottlenose dolphin, and sperm whale). Fossil-calibrated phylogenetic analysis, based on 1,915 single-copy gene families, revealed that S. chinensis and the bottlenose dolphin diverged ~4.8 million years ago (Figure S7).

As S. chinensis represents the first chromosome-level assembly of a 22-chromosome cetacean, we reconstructed the ancestral chromosomes of toothed whales as well as the ancestor of cetaceans and ruminants (Cetruminantia). The evolution of chromosomes is an important driver of speciation and diversification (White, 1969). It is well established that genomic structural rearrangements (often manifested as chromosome copy number variation stemming from fusions, fissions, and translocations) offer valuable insights into the diversification across macroevolutionary scales (Kim et al., 2017; O’Connor et al., 2018a, 2018b; Zhang et al., 2014). These rearrangements can result in the generation of novel genes or transcripts, as well as allowing the co-regulation of previously distantly located genes (Mertens et al., 2015). Cetacea and even-toed ungulates (Artiodactyla) evolved from a common terrestrial ancestor (Cetartiodactyla) over 55 million years ago (Berta et al., 2015); however, across extant species, there are substantial differences in the range of chromosome numbers between Cetacea (n = 21–22) and terrestrial Artiodactyla (n = 3–37) (ÁRnason, 1974; Graphodatsky et al., 2011; Kim et al., 2017; Rubes et al., 2012; Wurster and Benirschke, 1970). Previous studies made efforts to characterize the ancestral karyotype of Cetartiodactyla by relying on molecular cytogenetics (Rubes et al., 2012) and cross-species chromosome painting (Balmus et al., 2007; Kulemzina et al., 2009). A recent study, employing cross-species BAC mapping to the cattle X chromosome, revealed synteny blocks and rearrangements within Cetartiodactyla and a preliminary reconstruction of the ancestral X chromosome (Proskuryakova et al., 2017). However, the evolutionary history of ancient and recent chromosome rearrangements leading to extant cetaceans remains largely unexplored by using chromosome-level genome assemblies (Kim et al., 2017). Therefore, we performed synteny analysis using the genome of S. chinensis (n = 22), sperm whale (Physeter macrocephalus, n = 21), and cattle (Bos taurus, n = 30) (Figure 1A and Tables S6 and S7). This revealed evidence of extensive chromosomal rearrangements among them (Figures S8–S11).

Figure 1.

Figure 1

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Synteny between the Indo-Pacific Humpback Dolphin and Other Mammal Species

(A) Synteny of genome scaffolds of the Indo-Pacific humpback dolphin and cattle (Sousa chinensis and Bos taurus; red lines), Indo-Pacific humpback dolphin and sperm whale (S. chinensis and Physeter macrocephalus; green lines), and sperm whale and cattle (P. macrocephalus and B. taurus; blue lines).

(B) 342 shared homologous synteny blocks (HSBs) in the Indo-Pacific humpback dolphin (S. chinensis), cattle (B. taurus), sperm whale (P. macrocephalus), sheep (Ovis aries), and horse (Equus caballus).

Taking advantage of multiple high-quality chromosome-level assemblies for Cetartiodactyla (represented by sheep, cattle, sperm whale, and S. chinensis), as well as their sister group Perissodactyla (represented by the horse), we reconstructed the ancestral karyotypes of Cetruminantia, as well as the ancestors of Bovidae and Odontoceti. We identified 342 shared homologous synteny blocks (HSBs) (Murphy et al., 2005), covering 90.5%, 85.2%, 78.1%, 78.9%, and 83.8% of S. chinensis, sperm whale, sheep, cattle, and horse genomes, respectively (Figure 1B). Based on these HSBs, we reconstructed the ancestral chromosomes for Cetruminantia (28), Bovidae (30), and Odontoceti (22) (Tables S8–S10). This analysis confirmed that the number of ancestral chromosomes of Odontoceti is the same as that of most extant cetacean families (22 chromosome pairs) and different from that of superfamily Physeteroidea (ÁRnason, 1974) and family Ziphiidae (Kurihara et al., 2017) (21 chromosome pairs). Thus, we propose a model of chromosome evolution in cetaceans in which a chromosome fusion event likely occurred in the physeterids (i.e., sperm whales).

We detected 14 reshuffling events (including six fusions) in the lineage leading from the ancestral Cetruminantia to the Odontoceti ancestor, 32 in the S. chinensis lineage, and 42 in the sperm whale lineage. We identified 42 chromosome reshuffling events (including two fissions) in the common ancestor of Bovidae as well as five and eight chromosome reshuffling events in the cattle and sheep lineages, respectively (Tables S11, S12, S13, S14, S15, and S16). Thus, we confirmed a completely opposite karyotype evolution pattern between the lineage leading to the Odontoceti ancestor (reduced chromosome number) and the Bovidae ancestor (increased chromosome number).

Chromosome rearrangements can serve a functional purpose (Mérot et al., 2020). We identified seven fusions, 34 inversions, and 40 breakpoints during the evolution in the ancestral odontocete lineage (Figure 2). Such rearrangements in marine mammals could affect the function (e.g., regulation) of genes, thereby mediating adaptations to an aquatic environment. To explore this phenomenon, we compared ancestral Cetruminantia to ancestral Odontoceti and ancestral Odontoceti to S. chinensis. When comparing Odontoceti and Cetruminantia, we found ten genes located in 4-kb flanking regions of the 40 breakpoints (Table S17). For example, adenylate cyclase type 1 (ADCY1; Sochi02981), which plays a role in kidney filtration (Xiao et al., 2011), is associated with distinct kidney structures of freshwater and marine finless porpoises (Zhou et al., 2018a). Coding variants of the sodium chloride symporter gene SLC12A3 (Sochi08789) are associated with reduced blood pressure in humans (Nandakumar et al., 2018). Glypican-3 precursor (GPC3; Sochi10755) plays a role in vertebrate limb patterning and skeletal development by controlling the cellular response to bone morphogenic protein 4 (BMP4) and may be related to the lack of hind limbs in cetaceans (Paine-Saunders et al., 2000; Saad et al., 2017).

Figure 2.

Figure 2

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Chromosome Evolution of Cetruminantia

Chromosomes from the same ancestral chromosome are in the same color. Blue lines denote translocations, red lines fusions, and green lines fissions.

Compared with the odontocete ancestor, we detected 105 inversions in S. chinensis (Figure 2). Six genes were located in 4-kb flanking regions of 138 breakpoints resulting from these HSBs (Table S18). One of these genes, SERPINB8 (Sochi06838), is involved in maintaining the mechanical stability of skin (Pigors et al., 2016). Loss of SERPINB8 in humans results in peeling skin syndrome, where the outermost layer of the epidermis peels off upon exposure to water or skin occlusion (Pigors et al., 2016). Some S. chinensis individuals in Chinese waters have pink skin, likely attributed to the dilation of subcutaneous blood vessels to get rid of excess body heat (Di Meglio et al., 2011). We speculate that SERPINB8 might mediate this adaptation, rendering S. chinensis more susceptible to physical damage, stressors, and pathogens in their present-day environments. S. chinensis is vulnerable to environmental pollutants and pathogens (Parsons, 1998; Parsons et al., 2001), threats likely to affect its immune system. Another gene in the breakpoint region is CDA (Sochi00142), a gene encoding a modulator of innate immunity (Furusho et al., 2018; Liu et al., 2018b).

Ecologically, S. chinensis is distributed in several large estuarine areas within Chinese waters: the west coast waters of Taiwan, Xiamen waters, the Pearl River estuary, the southwest waters of Hainan Island, Leizhou Bay (hereafter LZB), and Sanniang Bay (hereafter SNB) (Chen et al., 2009, 2018a; Hemami et al., 2018; Huang et al., 2012; Jefferson and Smith, 2016; Li et al., 2016; Wang et al., 2012; Xu et al., 2015). To gain insights into the demographic history and population genetic status of S. chinensis, we sequenced 39 individuals (at an average sequencing depth of ~30×) from two neighboring regions in Chinese waters (LZB and SNB) (Table S19). We reconstructed the demographic history of S. chinensis in various ways. First, the pairwise sequentially Markovian coalescent (PSMC) model analysis (Ne estimates reliable at 20 ka to 3 Ma, Li and Durbin, 2011) revealed the onset of a severe S. chinensis population decline during the Mid-Pleistocene Transition 1 mya (Figure 3A). Next, we estimated that the populations split at ~40 ka (38.1k ~ 42.2k, 95% confidence interval [CI]), a time with relatively large S. chinensis effective population sizes (LZB 2,939; SNB 15,233) (Figure 3B). This timing coincides with an alternating warm and wet period during the last glacial age, making the LZB and SNB available for colonization and gradual emergence of the two separate populations on either side of the Leizhou Peninsula (Zhong et al., 2010). After the population split, symmetric gene flow between the two populations was detected, suggesting there was still a relatively large genetic pool or mating opportunities between the two populations. This was followed by a marked bottleneck 3,837 (3,645–4,039, 95% CI) years ago, with effective population sizes (Ne) decreasing rapidly to 611 and 487 in LZB and SNB, respectively (Figure 3B, Tables S20 and S21). The bottleneck may be associated with the rapid temperature and sea level decline ~4,000 ago (Li, 2018; Li et al., 2017).

Figure 3.

Figure 3

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The Heterozygosity and Demographic History of Indo-Pacific Humpback Dolphins in the South China Sea

(A) Demographic histories of Indo-Pacific humpback dolphin populations using the PSMC model. The orange line denotes the LZB population; the green line denotes the SNB population. Settings: g (generation time) = 25 years; μ (neutral mutation rate per generation) = 5.81 × 10−9.

(B) DaDi analyses of Indo-Pacific humpback dolphin population models between LZB and SNB. We used the “sym_mig_size” model, under which two populations split with symmetric migration and then size change with symmetric migration. nu1a: size of population LZB after split. nu2a: size of population SNB after split. T1: time in the past of split. nu1b: size of LZB after time interval. nu2b: size of population SNB after time interval. T2: time of population size change. m: migration rate between populations.

(C) Effective population sizes (Ne) of LZB and SNB in recent time (100 generations before present; approximately 2,500 years). The orange line denotes the LZB population; the green line denotes the SNB population, with 90% confidence intervals for each population as dotted lines. (D) Comparison of heterozygosity between Leizhou Bay (LZB) and Sanniang Bay (SNB) populations and other mammals.

A decreased population size was supported by an approximate Bayesian computation method, PopSizeABC (Boitard et al., 2016), employed to better characterize the contemporary S. chinensis effective population size (Ne) dynamics over the last 100 generations. We found that both the LZB and the SNB populations declined over the last 2,500 years, with a contemporary Ne of 12 (11–15, 90% CI) in LZB and 8 in SNB (6–11, 90% CI), respectively (Figure 3C). The extraordinary low population estimate of these populations highlights the urgent need for efficient conservation and management efforts.

In addition, the nucleotide diversity (π) of S. chinensis (π: 0.00015 in LZB and 0.00016 in SNB; Figure S12) is much lower than the killer whale estimation (π = 0.0029) (Foote et al., 2016). We also found a relatively low mitochondrial DNA polymorphism (LZB: 0.0034 and SNB: 0.0038), with only 52 SNPs. The average heterozygosity of S. chinensis is 1.79 × 10−4, similar to the recently extinct baiji (1.21 × 10−4), but notably lower than the common bottlenose dolphins (14.2 × 10−4) and Yangtze finless porpoises (8.60 × 10−4) (Figure 3D and Table S22) (Yim et al., 2014; Yuan et al., 2018; Zhou et al., 2013, 2018a). As inbreeding is considered a potential cause of low diversity, we calculated the inbreeding coefficient (Fh) within the two S. chinensis populations (Wright, 1922), but found no evidence of inbreeding (Tables S23 and S24).

Early barriers to gene flow (introgression) such as geographic isolation are common drivers of speciation (Poelstra et al., 2014; Via, 2009). SNB and LZB clearly split into two populations isolated by the Leizhou Peninsula (Figures 4A–4D and S13). Furthermore, admixture analysis indicates that LZB subgroups exist (Figure 4B). This observation may reflect the pigmentation differences (Chen et al., 2018b) of individuals in this population (Figure S14); however, further studies are warranted. We found no evidence of gene flow between the LZB and SNB populations from f3 statistics (Reich et al., 2009) (Table S25). We next assessed the genetic differentiation between populations, and the overall fixation index (FST) was estimated to be ~0.138, indicating moderate differentiation. To reliably investigate positive selection in the LZB and SNB populations separately under the background of moderate differentiation, we integrated five different methods, including FST, Tajima's D, XP-CLR, XP-EHH, and the μ-statistic (Alachiotis and Pavlos, 2018; Chen et al., 2010; Danecek et al., 2011; Sabeti et al., 2007) (Figures S15 and S16). Finally, we identified seven putative regions with eight genes (CAMKK2, P2RX4, P2RX7, IFT81, ATP2A, OLA1, and KANSL2) in the LZB population (Table S26). Among those genes, CAMKK2 mediates pleiotropic responses to physiologic and pathophysiological processes (Marcelo et al., 2016; Racioppi and Means, 2012), P2RX4 and P2RX7 play critical roles in immunity and inflammation (Burnstock, 2016; Raouf et al., 2007), ATP2A is involved in the role of maintaining cytoplasmic calcium levels (Pegoraro et al., 2011), and OLA1 is involved in oxidative stress (Zhang et al., 2009). Correspondingly, in the SNB population, we identified four regions with five genes (two copies of TBC1D10A, CNTRL, C5, and THBS1) (Table S26). Among these genes, C5 and THBS1 are involved in the regulation of the innate immune response during infection (Noris and Remuzzi, 2013; Zhao et al., 2015). These results suggest that, although geographical isolation led to the differentiation between the two populations, natural selection also played a role in the adaptation to their respective habitats.

Figure 4.

Figure 4

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Population Characteristics of Indo-Pacific Humpback Dolphins

(A) Locations of Leizhou Bay (LZB) and Sanniang Bay (SNB) populations in the northwestern South China Sea.

(B) Population structure of 39 Indo-Pacific humpback dolphins, varying the number of admixture components (K) from 2 to 4. The sample location for each individual is indicated with a population-specific prefix (LZB or SNB).

(C) Principal-component analysis (PCA) of LZB and SNB Indo-Pacific humpback dolphins. In particular, the first eigenvector separated the two populations. (D) Phylogenetic tree of Indo-Pacific humpback dolphins from the LZB and SNB populations.

Our analyses suggest that the LZB and SNB populations experienced a severe genetic bottleneck and that there has been no migration after the populations split. Although genetic drift caused by a bottleneck is likely to be the dominant evolutionary mechanism driving population divergence between LZB and SNB populations, natural selection also played a role. Our results also suggest that the LZB and SNB populations are differentiating, which may be reflected in morphological differentiation. Indeed, evidence of recent morphological differentiation has been identified between other S. chinensis populations (Wang et al., 2015).

Discussion

The high-quality genome assembly of the Indo-Pacific humpback dolphin reported in this study enables a unique view of cetacean chromosome evolution. Although there have been numerous studies on cetacean genome evolution, including gene family expansions/contractions, genes under selection, and their possible roles in adaptation, our work is the first to consider evolution at the chromosome level using genomic data. We have established chromosome evolution from the common ancestor of Cetruminantia (28 chromosomes) to the ancestral Odontoceti (22 chromosomes), to S. chinensis (22 chromosomes). The ever-increasing number of chromosome-level genomes promises an increasingly more precise picture of the genomes of extant species and their ancestors. Finally, we reveal that S. chinensis population sizes in southern China are steadily decreasing, coupled with evidence of divergence of populations in close geographic proximity. The estimated worldwide population size of S. chinensis is less than 13,000 individuals (Huang et al., 2012; Jefferson et al., 2017), nearly half of which are in Chinese waters. This study emphasizes the urgency for effective conservation of the Indo-Pacific humpback dolphin, a Vulnerable species.

Limitations of the Study

We reported a high-quality assembly of the Indo-Pacific humpback dolphin. We deduced the chromosome reshuffle events from its cetruminant ancestor and identified 16 genes locating in breakpoint regions during the chromosome evolution, potentially related to an aquatic environment adaptation. More evidence is needed to firmly establish a functional role for these genes, however. Furthermore, samples from wider geographical locations are needed to fully capture the population history of the Indo-Pacific humpback dolphin.

Resource Availability

Lead Contact

Further information and requests for resources and reagents should be directed to and will be fulfilled by the Lead Contact, Songhai Li (lish@idsse.ac.cn).

Materials Availability

This study did not generate new unique reagents.

Data and Code Availability

The accession number for the Indo-Pacific humpback dolphin chromosomal genome assembly reported in this paper is CNGBdb: CNP0000397.

Methods

All methods can be found in the accompanying Transparent Methods supplemental file.

Acknowledgments

This work was financially supported by the Ocean Park Conservation Foundation, Hong Kong (Nos. MM03-1415, MM02-1516); the National Natural Science Foundation of China (No. 41422604); the Major Science and Technology Project of Hainan Province (Nos. ZDKJ2016009 and ZDKJ2019011); Chinese White Dolphin Conservation Action Project of and Rural Affairs of the People's Republic of China (No. Y760091HT1); the biodiversity investigation, observation and assessment program (2019–2023) of Ministry of Ecology and Environment, the People’s Republic of China; the Youth Innovation Promotion Association of Chinese Academy of Sciences; and the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA19060403).

Author Contributions

S.L. conceived and designed this study. P.Z., Y. Zhao, and C.L. performed sample preparation and sequencing. P.Z., M. Lin, K.L., M. Liu, and L.D. collected the samples for assembly and re-sequencing. R.Z. and X.L. performed genome assembly. Y. Zhang and Y. Zhao performed genome annotation. Y. Zhao, G.F., and I.S. performed analysis of evolution. C.L., Y. Zhao, R.Z., and H.Z. performed analysis of population. Y. Zhao, P. Z., G.F., X.L., and S.L. wrote the manuscript. All other authors reviewed and revised the manuscript.

Declaration of Interests

The authors declare no competing interests.

Published: October 23, 2020

Footnotes

Supplemental Information can be found online at https://doi.org/10.1016/j.isci.2020.101640.

Contributor Information

Guangyi Fan, Email: fanguangyi@genomics.cn.

Xin Liu, Email: liuxin@genomics.cn.

Songhai Li, Email: lish@idsse.ac.cn.

Supplemental Information

Document S1. Transparent Methods, Figures S1–S15, and Tables S1–S10, S17, S18, S20, and S22–S26
mmc1.pdf (4.3MB, pdf)
Table S11. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Cetruminantia to Ancestral Odontoceti, Related to Figure 2
mmc2.xlsx (10.8KB, xlsx)
Table S12. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Odontoceti to S. chinensis, Related to Figure 2
mmc3.xlsx (13.7KB, xlsx)
Table S13. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Odontoceti to P. macrocephalus, Related to Figure 2
mmc4.xlsx (12.3KB, xlsx)
Table S14. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Cetruminantia to Ancestral Bovidae, Related to Figure 2
mmc5.xlsx (14.2KB, xlsx)
Table S15. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Bovidae to B. taurus, Related to Figure 2
mmc6.xlsx (10.2KB, xlsx)
Table S16. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Bovidae to O. aries, Related to Figure 2
mmc7.xlsx (10.4KB, xlsx)
Table S19. Resequencing Information of 39 Indo-Pacific Humpback Dolphins, Related to Figure 3
mmc8.xlsx (13.7KB, xlsx)
Table S21. The 32 DaDi Models We Used to Determine Divergence Time and Migration Rates between Leizhou Bay and Sanniang Bay Populations, Related to Figure 3
mmc9.xlsx (13.2KB, xlsx)

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Document S1. Transparent Methods, Figures S1–S15, and Tables S1–S10, S17, S18, S20, and S22–S26
mmc1.pdf (4.3MB, pdf)
Table S11. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Cetruminantia to Ancestral Odontoceti, Related to Figure 2
mmc2.xlsx (10.8KB, xlsx)
Table S12. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Odontoceti to S. chinensis, Related to Figure 2
mmc3.xlsx (13.7KB, xlsx)
Table S13. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Odontoceti to P. macrocephalus, Related to Figure 2
mmc4.xlsx (12.3KB, xlsx)
Table S14. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Cetruminantia to Ancestral Bovidae, Related to Figure 2
mmc5.xlsx (14.2KB, xlsx)
Table S15. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Bovidae to B. taurus, Related to Figure 2
mmc6.xlsx (10.2KB, xlsx)
Table S16. The Most Parsimonious Scenarios for Evolutionary Changes from Ancestral Bovidae to O. aries, Related to Figure 2
mmc7.xlsx (10.4KB, xlsx)
Table S19. Resequencing Information of 39 Indo-Pacific Humpback Dolphins, Related to Figure 3
mmc8.xlsx (13.7KB, xlsx)
Table S21. The 32 DaDi Models We Used to Determine Divergence Time and Migration Rates between Leizhou Bay and Sanniang Bay Populations, Related to Figure 3
mmc9.xlsx (13.2KB, xlsx)

Data Availability Statement

The accession number for the Indo-Pacific humpback dolphin chromosomal genome assembly reported in this paper is CNGBdb: CNP0000397.

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