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The life aquatic: advances in marine vertebrate genomics

Key Points

  • Marine vertebrates are relatively understudied at the genomic level compared to their terrestrial counterparts. Closing this gap is of the utmost importance because marine vertebrates have key roles in marine ecosystems and are a major source of protein for humans worldwide.

  • Genomic resources have become accessible to more study systems owing to both the increase in molecular and computational techniques available for studying non-model organisms (such as reduced-representation and transcriptome sequencing) and the rapid decline in sequencing costs.

  • Recent studies comparing the genomes of marine vertebrates to terrestrial vertebrates have offered key insights into the process of adaptation to the marine environment. In particular, these studies have shown that many of the same pathways often underlie adaptation to the marine environment in different taxa.

  • Genes underlying morphological traits (HOX genes) remain largely conserved between marine and terrestrial sister taxa. Instead, less constrained cis-regulatory mutations have been found to underlie morphological evolution.

  • Marine environments often have a low cost of dispersal and few physical barriers to gene flow, and they support large populations. Despite these features, genomic analyses have identified structuring between subpopulations that other markers (such as mitochondrial control regions and microsatellites) have failed to detect.

  • Large populations in the ocean can harbour large pools of genetic diversity that can facilitate adaptation to new, different environments.

  • Marine vertebrates are at risk owing to climate change, overfishing, pollution and numerous other challenges. Genomics can help characterize both the responses to new stressors and the resiliency of a population.

Abstract

The ocean is hypothesized to be where life on earth originated, and subsequent evolutionary transitions between marine and terrestrial environments have been key events in the origin of contemporary biodiversity. Here, we review how comparative genomic approaches are an increasingly important aspect of understanding evolutionary processes, such as physiological and morphological adaptation to the diverse habitats within the marine environment. In addition, we highlight how population genomics has provided unprecedented resolution for population structuring, speciation and adaptation in marine environments, which can have a low cost of dispersal and few physical barriers to gene flow, and can thus support large populations. Building upon this work, we outline the applications of genomics tools to conservation and their relevance to assessing the wide-ranging impact of fisheries and climate change on marine species.

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Figure 1: Vast diversity in the marine environment.
Figure 2: Genome assemblies through the years.
Figure 3: Genomic insights into macroevolutionary transitions.
Figure 4: Genomic regions linked to local adaptation and associated with high population differentiation.

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Acknowledgements

J.L.K. and A.P.B. were supported in part by a grant from the US Army Research Office (W911NF-15-1-0175). A.D.F. was supported by a short visit grant from the European Science Foundation–Research Networking Programme ConGenOmics and by a Swisss National Science Foundation grant (31003A-143393) to L. Excoffier.

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FURTHER INFORMATION

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Glossary

Estuarine

An environment that is situated in the transition zone where the ocean meets rivers. One special challenge in this environment is that salt water from the ocean mixes with fresh water from a river, making this a unique environment in terms of salinity.

Coastal

An environment that is found near a shoreline and is shallower than most other marine environments; the substrates of the coast can vary considerably (sandy, rocky and so on).

Abyssal

An environment that is found in the deepest parts of the ocean. There is very little light and primary production, which makes it difficult for large predators to survive.

Macroevolution

Evolutionary patterns at or above the species level.

Microevolution

Evolutionary patterns at the population or subpopulation level.

Adaptation

The process by which populations become better at reproducing and surviving within a particular environment; this is a population-level process that typically involves changes in allele frequencies.

Effective population size

The number of breeding individuals within a population that contribute offspring to the next generation.

Clines

Gradients of environmental differences.

Cetaceans

A group that encompasses the fully aquatic marine mammals (including whales, dolphins and porpoises). The closest living terrestrial relative is the hippopotamus.

Pinniped

An organism that belongs to the group Pinnepedia, which encompasses all types of seals (including walruses, sea lions and fur seals). The closest living terrestrial relatives are bears.

Sirenian

An organism that belongs to the order Sirenia, which includes herbivorous marine mammals (such as dugongs and manatees). The closest living terrestrial relatives are elephants.

Pseudogenized

The process by which a functional gene becomes dysfunctional (a pseudogene) owing to sequence alterations such as premature stop codons. Pseudogenization during evolution often results in one species lineage harbouring the defective gene, whereas other species retain the functional homologue.

Otolith

A structure in the inner ear that helps marine vertebrates with balance and sound detection.

Pleiotropic

A phenomenon in which one gene has an effect on several, often seemingly unrelated, traits.

Benthic

The zone at the bottom of a body of water.

Euryhaline

Able to tolerate a wide range of salinity.

Synteny

The preserved order of genes on chromosomes of related species.

Panmixia

Random mating within a population.

Population structure

Differences in allele frequencies among subpopulations within a larger population, possibly due to different ancestry, inbreeding and so on.

Allozyme

Allelic variants of proteins detected by protein electrophoresis.

Standing genetic variation

Allelic variation that is currently segregating within a species, as opposed to alleles that arise through new mutations.

Selective sweeps

Processes by which new favourable mutations and physically linked alleles increase in frequency within a population owing to selection on the adaptive mutation, thereby reducing variation within a genomic region.

Genetic drift

A change in allele frequency due to random chance; small populations are especially susceptible to large changes in allele frequency resulting from genetic drift.

Identical-by-descent

Segments of DNA in multiple individuals that are derived from the same common ancestor.

Metagenomic analyses

Studies of DNA from multiple organisms that are found in environmental samples.

Hologenomes

The collective genomes of a host plus all of its symbiotic microbes.

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Kelley, J., Brown, A., Therkildsen, N. et al. The life aquatic: advances in marine vertebrate genomics. Nat Rev Genet 17, 523–534 (2016). https://doi.org/10.1038/nrg.2016.66

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