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Department of Zoology

 

I am passionate about the evolution of morphological diversity. What are the genes, mutations and developmental mechanisms responsible for the emergence of morphological variation? To answer this question we combine developmental genetics, quantitative and population genetics approaches using Lake Malawi cichlid fishes as a model system.

Mechanisms underlying the emergence and diversification of pigmentation patterns: The pigmentation patterns of lake Malawi cichlid fishes provide an ideal system to study morphological evolution. We specifically focus on a set of brightly pigmented spots on male anal fins, known as “egg-spots”. Egg-spots are a diverse trait (number, colour and shape), and play a key role in the territorial and breeding behaviour of around 1,500 species of cichlids. They are relatively simple structure, consisting of a circular area made up of xanthophores and iridophores (orange and silver pigment cells respectively) and are often surrounded by a transparent outer-ring. With the availability of hundreds of cichlid species genomes and genome editing tools (eg. Tol2 transgenesis and CRISPR), we can link genetics, cellular biology, development, to organismal trait variation. By addressing these mechanisms across different timescales (populations, species and genera) we can also tackle a long-standing question: whether the basis of adaptive change is the same at the micro- and macro-evolutionary scale. 

 

Neural crest cell development and evolution in cichlid fishes: Neural crest cells are a multipotent embryonic cell population that emerge from the vertebrate dorsal neural tube during early development. They then delaminate and undergo some of the longest migrations of any embryonic cell type to give origin to multiple derivatives such as pigment cells, neurons and glia of the peripheral nervous system, smooth muscle, craniofacial cartilage and bone. Many of the features that distinguish vertebrates from their chordate relatives are derived from the neural crest, making this multipotent embryonic cell population a key innovation central to vertebrate evolution. The origin and development of the neural crest has been extensively studied in a handful of model organisms (e.g. lamprey, zebrafish, frog and chicken). Most work focusing on the gene regulatory networks and developmental mechanisms associated with NC specification and differentiation, together with the examination of how one stem cell population can migrate so extensively to different parts of the vertebrate body plan and diversify into multiple cell types. However, we still do not know how variation in NC genetic and developmental mechanisms underlie the subtle variation in NC derived morphologies (e.g. craniofacial skeleton and pigmentation) present within a population and between closely related species. We are currently addressing this using cichlid natural variation to identify genes and cellular mechanisms generating variation during NC development.

Publications

Key publications: 

 

- Clark B, Elkin J, Marconi A, Turner GF, Smith AM, Joyce D, Miska EA, Juntti SA, Santos ME (2022) oca2 targeting using CRISPR/Cas9 in the Malawi cichlid Astatotilapia calliptera. bioRxiv, doi.org/10.1101/2022.01.01.474687

- Elkin J, Martin A, Courtier-Orgogozo V, Santos ME (2022) Meta-analysis of the genetic loci of pigment pattern evolution in vertebrates. bioRxiv, doi.org/10.1101/2022.01.01.474697

- Santos ME, Le Bouquin A, Crumière AJJ, Khila A (2017) Taxon-restricted genes at the origin of morphological novelty and ecological opportunity in water striders. Science, 358:386-390

- Santos ME, Baldo L, Gu X, Boileau N, Musilova Z, Salzburger W (2016) Comparative transcriptomics of anal fin pigmentation patterns in cichlid fishes. BMC Genomics, 17: 712.

- Santos ME, Berger C, Refki P, Khila A (2015) Integrating evo-devo with ecology for a better understanding of phenotypic evolution. Briefings in Functional Genomics, 14:384-395.

- Santos ME, Braasch I, Boileau N, Meyer B, Boehne A, Affolter M, Salzburger W (2014) The evolution of cichlid egg-spots are linked with a cis-regulatory change. Nature Communications, 5:5149.

- Santos ME, Salzburger W (2012) How cichlids diversify. Science, 338:619-621.

- Santos ME, Athanasiadis A, Leitão AB, Dupasquier L, Sucena E (2011) Alternative splicing and gene duplication in the evolution of the FoxP gene sub-family. Molecular Biology and Evolution, 28:237-47.

 

Other publications: 

 

- Vernaz G, Hudson AG, Santos ME, Fisher B, Carruthers M, Shechonge AH, Gabagambi NP, Tyers AM, Ngatunga BP, Malinsky M, Durbin R, Turner GF, Genner MJ, Miska EA (2021) Epigenetic divergence during early stages of speciation in african crater lake cichlid fish. bioRxiv, doi.org/10.1101/2021.07.30.435319 under review in Nature Ecology and Evolution.

- Munby H, Linderoth T, Fisher B, Du M, Vernaz G, Tyers AM, Ngatunga BP, Shechonge A, Denise H, McCarthy SA, Bista I, Miska EA, Santos ME, Genner MJ, Turner GF, Durbin R (2021) Differential use of multiple genetic sex determination systems in divergent ecomorphs of an african crater lake cichlid. bioRxiv, doi.org/10.1101/2021.08.05.455235 under review in elife.

- Vernaz G, Malinsky M, Svardal H, Du M, Tyers AM, Santos ME, Durbin R, Genner MJ, Turner GF, Miska EA (2021) Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes. Nature Communications, 12:5870

- Svardal H, Rusuwa B, Linderoth T, Kiran A, Charmantier A, Lattorff HMG, Cagan A, Ommeh SC, Kamng’ona A, Katong C, Santos ME, Durbin R, Kumwenda B, Visscher PM, von der Heyden S, and the Participants of  SMBE Malawi (2020) Evolutionary Genomics at the Human-Environment Interface in Africa. Molecular Biology and Evolution, 10: 3076-3080

- Vargas-Lowman A, Armisen D, Floriano CFB, Silva Cordeiro IR, Viala S, Bouchet M, Bernard M, Le Bouquin A, Santos ME, Berlioz-Barbier A, SalvadorA, Moreira FFF, Bonneton F, Khila A (2019) Cooption of the pteridine biosynthesis pathway underlies the diversification of embryonic colors in water striders. PNAS, 116:19046-19054.

- Souza da Motta F, Moreira FFF, Crumière AJJ, Santos ME, Khila A (2018) A new species of Rhagovelia Mayr, 1865 (Hemiptera: Heteroptera: Veliidae) from French Guiana, with new records of Gerromorpha from the the country. Zootaxa, 4433:520-530

- Santos ME (2017) One gene, multiple alleles: insights into the microevolution of pigmentation patterns. Molecular Ecology 26:2605-2607

- Crumière AJJ, Santos ME, Sémon M, Armisén D, Moreira FFF, and Khila A (2016) Diversity in morphology and locomotory behavior is associated with niche expansion in the semi-aquatic bugs. Current Biology, 26:3336-3342

- Colombo M, Diepeveen ET, Muschick M, Santos ME, Indermaur A, Boileau N, Barluenga M, Salzburger W (2013) The ecological and genetic basis of convergent thick-lipped phenotypes in cichlid fishes. Molecular Ecology, 22:670-684.

- Baldo L, Santos ME, Salzburger W (2011) Comparative transcriptomics of Eastern African cichlid fishes shows signs of positive selection and a large contribution of untranslated regions to genetic diversity. Genome Biology and Evolution, 3:443-55.

- Lopes PC, Sucena E, Santos ME, Magalhães S (2008) Rapid experimental evolution of pesticide resistance in C. elegans entails no costs and affects the mating system. PLoS ONE, 3(11): e3741.

 

Genome consortium publications

- Panfilio KA, Vargas Jentzsch IM, Benoit JB [ and 78 other, including Santos ME] (2019) Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. Genome Biology, 20: 64.

- Armisen D, Rjakuma R, Friedrich M [ and 51 other, including Santos ME] (2018) The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to live on the water. BMC Genomics, 19: 832.

- Adelman Z, Reinhardt K, Dolan A, [ and 77 other, including Santos ME] (2016) Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nature Communications, 7:10165.

- Brawand D, Wagner CE, Li YI, [ and 72 other, including Santos ME] (2014) The genomic substract for adaptive radiation in African cichlid fish. Nature, 513:375-381.

 

NERC Independent Research Fellow
Assistant Professor

Contact Details

Room No: 2.01
DAB
01223 (3)36678
Accepting applications for PhD students.