The Genomic Basis of Cichlid Fish Adaptation Within the Deepwater "twilight Zone" of Lake Malawi

Overview

Journal Evol Lett

Publisher Oxford University Press

Specialty Biology

Date 2018 Oct 5

PMID 30283648

Citations 12

Authors

Christoph Hahn

Martin J Genner

George F Turner

Domino A Joyce

Affiliations

Soon will be listed here.

Abstract

Deepwater environments are characterized by low levels of available light at narrow spectra, great hydrostatic pressure, and low levels of dissolved oxygen-conditions predicted to exert highly specific selection pressures. In Lake Malawi over 800 cichlid species have evolved, and this adaptive radiation extends into the "twilight zone" below 50 m. We use population-level RAD-seq data to investigate whether four endemic deepwater species ( spp.) have experienced divergent selection within this environment. We identify candidate genes including regulators of photoreceptor function, photopigments, lens morphology, and haemoglobin, many not previously implicated in cichlid adaptive radiations. Colocalization of functionally linked genes suggests coadapted "supergene" complexes. Comparisons of to the broader Lake Malawi radiation using genome resequencing data revealed functional substitutions and signatures of positive selection in candidate genes. Our data provide unique insights into genomic adaptation within deepwater habitats, and suggest genome-level specialization for life at depth as an important process in cichlid radiation.

Citing Articles

Dynamic Outlier Slicing Allows Broader Exploration of Adaptive Divergence: A Comparison of Individual Genome and Pool-Seq Data Linked to Humic Adaptation in Perch.

Lopez M, Ozerov M, Pukk L, Noreikiene K, Gross R, Vasemagi A Mol Ecol. 2025; :e17659.

PMID: 39846218 PMC: 11815547. DOI: 10.1111/mec.17659.

A whole-body micro-CT scan library that captures the skeletal diversity of Lake Malawi cichlid fishes.

Bucklow C, Genner M, Turner G, Maclaine J, Benson R, Verd B Sci Data. 2024; 11(1):984.

PMID: 39256465 PMC: 11387623. DOI: 10.1038/s41597-024-03687-1.

New chromosome-scale genomes provide insights into marine adaptations of sea snakes (Hydrophis: Elapidae).

Ludington A, Hammond J, Breen J, Deveson I, Sanders K BMC Biol. 2023; 21(1):284.

PMID: 38066641 PMC: 10709897. DOI: 10.1186/s12915-023-01772-2.

Visual opsin gene expression evolution in the adaptive radiation of cichlid fishes of Lake Tanganyika.

Ricci V, Ronco F, Boileau N, Salzburger W Sci Adv. 2023; 9(36):eadg6568.

PMID: 37672578 PMC: 10482347. DOI: 10.1126/sciadv.adg6568.

Sexual imprinting leads to speciation in locally adapted populations.

Sibly R, Curnow R Ecol Evol. 2022; 12(11):e9479.

PMID: 36381395 PMC: 9643133. DOI: 10.1002/ece3.9479.

References

Twigg S, Versnel S, Nurnberg G, Lees M, Bhat M, Hammond P . Frontorhiny, a distinctive presentation of frontonasal dysplasia caused by recessive mutations in the ALX3 homeobox gene. Am J Hum Genet. 2009; 84(5):698-705. PMC: 2681074. DOI: 10.1016/j.ajhg.2009.04.009. View

Parsons K, Trent Taylor A, Powder K, Albertson R . Wnt signalling underlies the evolution of new phenotypes and craniofacial variability in Lake Malawi cichlids. Nat Commun. 2014; 5:3629. PMC: 4238940. DOI: 10.1038/ncomms4629. View

Coop G, Witonsky D, Di Rienzo A, Pritchard J . Using environmental correlations to identify loci underlying local adaptation. Genetics. 2010; 185(4):1411-23. PMC: 2927766. DOI: 10.1534/genetics.110.114819. View

Liu B, Rooker S, Helms J . Molecular control of facial morphology. Semin Cell Dev Biol. 2009; 21(3):309-13. PMC: 3410822. DOI: 10.1016/j.semcdb.2009.09.002. View

Sivasundar A, Palumbi S . Parallel amino acid replacements in the rhodopsins of the rockfishes (Sebastes spp.) associated with shifts in habitat depth. J Evol Biol. 2010; 23(6):1159-69. DOI: 10.1111/j.1420-9101.2010.01977.x. View

Delahunt P, Webster M, Ma L, Werner J . Long-term renormalization of chromatic mechanisms following cataract surgery. Vis Neurosci. 2004; 21(3):301-7. PMC: 2633455. DOI: 10.1017/s0952523804213025. View

Hancock A, Witonsky D, Alkorta-Aranburu G, Beall C, Gebremedhin A, Sukernik R . Adaptations to climate-mediated selective pressures in humans. PLoS Genet. 2011; 7(4):e1001375. PMC: 3080864. DOI: 10.1371/journal.pgen.1001375. View

Wen W, Pillai-Kastoori L, Wilson S, Morris A . Sox4 regulates choroid fissure closure by limiting Hedgehog signaling during ocular morphogenesis. Dev Biol. 2015; 399(1):139-153. PMC: 4339509. DOI: 10.1016/j.ydbio.2014.12.026. View

Oka M, Kudo H, Sugama N, Asami Y, Takehana M . The function of filensin and phakinin in lens transparency. Mol Vis. 2008; 14:815-22. PMC: 2358922. View

10.

Ivory S, Blome M, King J, McGlue M, Cole J, Cohen A . Environmental change explains cichlid adaptive radiation at Lake Malawi over the past 1.2 million years. Proc Natl Acad Sci U S A. 2016; 113(42):11895-11900. PMC: 5081594. DOI: 10.1073/pnas.1611028113. View

11.

Jennings R, Etter R, Ficarra L . Population differentiation and species formation in the deep sea: the potential role of environmental gradients and depth. PLoS One. 2013; 8(10):e77594. PMC: 3788136. DOI: 10.1371/journal.pone.0077594. View

12.

Wang F, Tang M, Yan H . A comparative study on the visual adaptations of four species of moray eel. Vision Res. 2011; 51(9):1099-108. DOI: 10.1016/j.visres.2011.02.025. View

13.

Brown T, Gias C, Hatori M, Keding S, Semo M, Coffey P . Melanopsin contributions to irradiance coding in the thalamo-cortical visual system. PLoS Biol. 2010; 8(12):e1000558. PMC: 2998442. DOI: 10.1371/journal.pbio.1000558. View

14.

Gribble S, Kim H, Bonner J, Wang X, Dorsky R . Tcf3 inhibits spinal cord neurogenesis by regulating sox4a expression. Development. 2009; 136(5):781-9. PMC: 2685945. DOI: 10.1242/dev.027995. View

15.

Gaston-Massuet C, McCabe M, Scagliotti V, Young R, Carreno G, Gregory L . Transcription factor 7-like 1 is involved in hypothalamo-pituitary axis development in mice and humans. Proc Natl Acad Sci U S A. 2016; 113(5):E548-57. PMC: 4747739. DOI: 10.1073/pnas.1503346113. View

16.

Yang Z, Peachey N, Moshfeghi D, Thirumalaichary S, Chorich L, Shugart Y . Mutations in the RPGR gene cause X-linked cone dystrophy. Hum Mol Genet. 2002; 11(5):605-11. DOI: 10.1093/hmg/11.5.605. View

17.

Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R . InterProScan: protein domains identifier. Nucleic Acids Res. 2005; 33(Web Server issue):W116-20. PMC: 1160203. DOI: 10.1093/nar/gki442. View

18.

Star B, Nederbragt A, Jentoft S, Grimholt U, Malmstrom M, Gregers T . The genome sequence of Atlantic cod reveals a unique immune system. Nature. 2011; 477(7363):207-10. PMC: 3537168. DOI: 10.1038/nature10342. View

19.

Nichols P, Genner M, Van Oosterhout C, Smith A, Parsons P, Sungani H . Secondary contact seeds phenotypic novelty in cichlid fishes. Proc Biol Sci. 2014; 282(1798):20142272. PMC: 4262179. DOI: 10.1098/rspb.2014.2272. View

20.

Miranda G, Abrahan C, Politi L, Rotstein N . Sphingosine-1-phosphate is a key regulator of proliferation and differentiation in retina photoreceptors. Invest Ophthalmol Vis Sci. 2009; 50(9):4416-28. DOI: 10.1167/iovs.09-3388. View