Genomes of endangered great hammerhead and shortfin mako sharks reveal historic population declines and high levels of inbreeding in great hammerhead

Stanhope, Michael J.; Ceres, Kristina; Sun, Qi; Wang, Minghui; Zehr, Jordan D; Marra, Nicholas J.; Wilder, Aryn P.; Zou, Cheng; Bernard, Andrea M.; Pavinski-Bitar, Paulina; Lokey, Mitchell G.; Shivji, Mahmood S.

doi:10.1016/j.isci.2022.105815

Cited by 14 publications

(10 citation statements)

References 68 publications

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“…2 B). The length gradualism is a remarkable feature of elasmobranch karyotypes, although we tentatively grouped those chromosomes into three length-dependent categories as proposed recently for other elasmobranch species ( Marlétaz et al 2023 ; Stanhope et al 2023 ). The pattern in the shark chromosomal organization is unique in its diversity among vertebrates ( Uno et al 2020 ), which is characterized by abundant chromosomes (up to 106 for diploids) and variable chromosome sizes.…”

Section: Discussionmentioning

confidence: 70%

Elasmobranch genome sequencing reveals evolutionary trends of vertebrate karyotype organization

Yamaguchi,

Uno,

Kadota

et al. 2023

Genome Res.

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Genomic studies of vertebrate chromosome evolution have long been hindered by the scarcity of chromosome-scale DNA sequences of some key taxa. One of those limiting taxa has been the elasmobranchs (sharks and rays), which harbor species often with numerous chromosomes and enlarged genomes. Here, we report the chromosome-scale genome assembly for the zebra sharkStegostoma tigrinum, an endangered species that has a relatively small genome among sharks (3.71 Gb), as well as for the whale sharkRhincodon typus. Our analysis employing a male-female comparison identified an X Chromosome, the first genomically characterized shark sex chromosome. The X Chromosome harbors the Hox C cluster whose intact linkage has not been shown for an elasmobranch fish. The sequenced shark genomes exhibit a gradualism of chromosome length with remarkable length-dependent characteristics—shorter chromosomes tend to have higher GC-content, gene density, synonymous substitution rate, and simple tandem repeat content as well as smaller gene length and lower interspersed repeat content. We challenge the traditional binary classification of karyotypes as with and without so-called microchromosomes. Even without microchromosomes, the length-dependent characteristics persist widely in some other vertebrate lineages. Our investigation of elasmobranch karyotypes underpins their unique characteristics and provides clues for understanding how vertebrate karyotypes accommodate intragenomic heterogeneity to realize a complex readout. It also paves the way to dissecting more genomes with variable sizes to be sequenced on high quality.

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Section: Discussionmentioning

confidence: 70%

Elasmobranch genome sequencing reveals evolutionary trends of vertebrate karyotype organization

Yamaguchi,

Uno,

Kadota

et al. 2023

Genome Res.

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“…The length and number of runs of homozygosity (ROHs) in a genome reflect the level of inbreeding and can provide conservation management guidance 110,111 . Longer ROHs suggest recent inbreeding.…”

Section: Resultsmentioning

confidence: 99%

Sirenian genomes illuminate the evolution of fully aquatic species within the mammalian superorder Afrotheria

Tian,

Zhang,

Kang

et al. 2023

Preprint

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Sirenians of the diverse superorder Afrotheria were the first mammals to retransition from land to water and are the sole herbivorous marine mammals, but little is known about the underlying genomic changes. Here, we generated a chromosome-level dugong (Dugong dugon) genome. A comparison of our assembly and a recent West Indian manatee genome with other afrotherian genomes revealed possible molecular solutions to aquatic life by sirenians, including a shift in daily activity patterns (circadian clock) and tolerance to a high-iodine plant diet mediated through changes in the iodide transporter NIS (SLC5A5) and its co-transporters. Functional in vitro assays confirmed that sirenian amino acid substitutions alter the properties of the circadian clock protein PER2 and NIS. Sirenians show evidence of convergent regression of integumentary system (skin and its appendages) genes with cetaceans, the only other fully aquatic mammal group. Our analysis also uncovered gene losses that may be maladaptive in a modern environment, including a candidate gene (KCNK18) for sirenian cold stress syndrome likely lost during their evolutionary shift in daily activity patterns. Finally, genomes from nine Australian locations and the functionally extinct Okinawan population confirm and date a genetic break on the Australian east coast and highlight the need for whole-genome resequencing data from small or isolated dugong populations worldwide for conservation and genetic management.

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“…Genetic and genomic tools provide a fantastic opportunity to explore these problems (Bertola et al, 2024; Funk et al, 2012; Stapley et al, 2010) and are increasingly being applied to elusive marine megafauna (Kelley et al, 2016). For example, recent work has uncovered contrasting patterns of genetic diversity in two recently diverged manta ray (Mobulidae) species (Humble et al, 2024), signals of inbreeding in great hammerhead sharks ( Sphyrna mokarran ) (Stanhope et al, 2023) and subtle stock structure in blue shark ( Prionace glauca ) – a species previously thought to comprise a single global population (Nikolic et al, 2023). These insights all have the potential to influence management through highlighting populations in need of prioritisation, feeding into non-detriment findings under the Convention on International Trade of Endangered Species of Wild Flora and Fauna (CITES) and informing fisheries management (Casey et al, 2016; Domingues et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Population structure and genetic diversity of the Critically Endangered bowmouth guitarfish (Rhina ancylostomus) in the Northwest Indian Ocean

Kipperman,

Jabado,

Haque

et al. 2024

Preprint

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The bowmouth guitarfish (Rhina ancylostomus) is a unique and relatively understudied species of wedgefish with a distribution spanning the Indo-Pacific Oceans. Due to targeted and bycatch fisheries, this species is experiencing serious declines across its range. It is now considered among the most threatened species of elasmobranch. Despite this, species-specific management is limited, particularly around primary fishing hotspots. This is in part due to knowing very little about fundamental population processes. Here, we combine mitochondrial and single nucleotide polymorphism (SNP) data to carry out the first genetic assessment ofR. ancylostomusacross the Northwest Indian Ocean. We find evidence for population structure across the species' northwest range that is best explained by dispersal constraints and therefore emphasises the importance of habitat connectivity. We also uncover a cline in genetic variation from east to west of the sampling distribution and identify regions in potential need of heightened protection. In doing so, our study provides baseline information to support conservation management ofR. ancylostomusand highlights the value of genomic data in elasmobranch conservation.

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Genomes of endangered great hammerhead and shortfin mako sharks reveal historic population declines and high levels of inbreeding in great hammerhead

Cited by 14 publications

References 68 publications

Elasmobranch genome sequencing reveals evolutionary trends of vertebrate karyotype organization

Elasmobranch genome sequencing reveals evolutionary trends of vertebrate karyotype organization

Sirenian genomes illuminate the evolution of fully aquatic species within the mammalian superorder Afrotheria

Population structure and genetic diversity of the Critically Endangered bowmouth guitarfish (Rhina ancylostomus) in the Northwest Indian Ocean

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