【News&Highlight】Genome sequences reveal global dispersal routes and suggest convergent genetic adaptations in seahorse evolution

GENOME EVOLUTION

nature
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Genome sequences reveal global dispersal routes and suggest convergent genetic adaptations in seahorse evolution

PacBio | Illumina | Hi-C | WGS | Genetic Diversity | Demographic History | Gene Flow

The Pacbio sequencing, genome de novo assembly and annotation services were provided by Biomarker Technologies.

Highlights

 

  1. A high quality chromosome-level seahorse (Hippocampus erectus) genome with contig N50 of 15.5 Mb was obtained.
  2. A total of 358 genomes from worldwide 21 seahorse species were resequenced.
  3. Seahorses evolved in the late Oligocene and subsequent circum-global colonization routes are identified and linked to changing dynamics in ocean currents and paleotemporal seaway openings
  4. The genetic basis of the recurring “bony spines” adaptive phenotype is linked to independent substitutions in a key developmental gene.
  5. Rafting via ocean currents compensates for poor dispersal and rapid adaptation facilitates colonizing new habitats

 

Achievements

Fig. 1 Genetic diversity and phylogenetic relationships of 358 seahorse specimens

a Geographic sampling locations for sampled seahorses with patterns of nucleotide diversity (π) of the 21 seahorse species across 22 chromosomes. b Neighborjoining tree constructed with genome-wide SNPs of 358 seahorses. Location pin symbols in (a) and branch background in (b) correspond to each other.

Fig. 2 Colonization and demographic history of seahorses

a Phylogenetic tree and divergence time estimates for 21 seahorse species. The branch line thickness corresponds to the population size estimates (Ne) and colors indicate different lineages. Symbols I–III indicate calibration points. b–d Predicted colonization routes (colored arrows) of seahorses based on divergence time, distribution, vicariance events, and ocean currents (white arrows). b The Indo-Australian Archipelago was the center of origin (red marking) of the genus Hippocampus before seahorses diversified and dispersed globally 18–23 Ma. c Seahorses initially colonized the Atlantic Ocean through the opening Tethyan seaway, which, after its closure (Terminal Event during 7–13 Ma), separated this Tethyan lineage from its Indian Ocean sister lineage. The latter, subsequently rapidly diversified (yellow marking) in the Arabian Sea, establishing a second center of seahorse diversification. d A second seahorse colonization event of the Atlantic Ocean occurred from the Indian Ocean about 5Ma by passing the South African tip, and finally arriving in the East Pacific Ocean through the still open Panama seaway approximately 3.6 Ma.

Fig. 3 Gene flow and fluctuations in the effective population size

a Gene flow detected between species inhabiting the South Atlantic Ocean. Gene flow is shown nearby the white lines as migration rate deduced by G-PhoCS. Thickness and direction of the arrows correspond to rates and direction of gene flow, respectively. b Fluctuations in effective population size by PSMC. The x axis represents time in years before present while the y axis represents the effective population size. The charts are organized mainly according to the geographic distribution for each of the species with different distribution areas. c Sea level change during the past 1 million years in meters33. The yellow line indicates the last global interglacial peak while the cyan shade indicates the last glacial maximum period.

Fig. 4 The evolution of spines.

a Left, Species tree displaying the independent evolution of spines in seahorses. The branch length indicates number of substitutions per site. Four spiny seahorse species are highlighted in blue. Thicker branches correspond to higher rates of nonsynonymous-to-synonymous substitutions (dN/dS) for bmp3 gene. Canonical and generalized McDonald and Kreitman test (MKT) for bmp3 gene was performed for three pairwise sister species with divergent spiny and non-spiny features highlighted by background colors, whose significance levels were indicated by p value with blue and red font, respectively. Right, comparison of amino acid substitutions in bmp3 protein, polymorphic and fixed substitutions in spiny seahorses are indicated with red and blue circles, respectively. b Distribution of dN/dS values in bmp3 in spiny seahorses compared to non-spiny species. c Independent evolution in the phylogenetic tree reconstructed for the protein encoded by bmp3. d Whole-mount in situ hybridization of bmp3 in Hippocampus erectus.

Reference

Li C et al. Genome sequences reveal global dispersal routes and suggest convergent genetic adaptations in seahorse evolution. Nat Commun. 2021 Feb 17;12(1):1094.

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