Intra-island diversification in the Reunion Gray White-eye

Remote oceanic islands provide unique scenarios in which to study the factors involved in population divergence and the formation of new species. The Reunion gray white-eye (Zosterops borbonicus) shows a striking, geographically structured plumage polymorphism on the topographically and ecologically complex yet small island of Reunion. In contrast, its sister species (Z. mauritianus) is monomorphic on the relatively uniform island of Mauritius. In collaboration with Christophe Thébaud (http://thebaud.weebly.com/) at the University of Toulouse, we are using various genetic, genomic and phenotypic analyses to investigate the evolutionary history of this unique intra-island radiation. We are specifically interested in the relative roles of vicariant barriers (mountains, rivers), ecological factors (altitudinal and ecological gradients) and sexual selection, in driving the process of divergence among populations. Our work is funded in part by France’s Agence Nationale de la Recherche (ANR) and National Geographic Society.

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Zosterops borbonicus forms

To date, our data for Reunion reveal marked genetic structure across the island, apparently driven by selection acting on very specific regions of the genome. A preliminary tree based on 20,000 SNP (single-nucleotide polymorphism) loci obtained by RADseq (restriction-site associated DNA sequencing), reveals that Z. borbonicus is divided into two main clades corresponding to ecologically different highlands and lowlands. In turn, the three lowland morphs (lowland brown, gray-headed brown, and gray-headed brown-naped) also form independent genetic lineages within the lowland clade.

Thus our genetic and morphometric results for Reunion show the early role of ecology in dividing populations into highland and lowland forms, and the existence of independent lineages in the lowlands suggests the existence of premating isolating barriers to reproduction, perhaps due to sexual selection on plumage traits. Despite being good flyers, our results indicate that dispersal in the gray white-eye is extremely limited and suggest the role of selection in restricting gene flow between incipient evolutionary lineages.

Check out this little video that Boris Delahaie and I put together on the project!:

Related publications:

 

Mould, M. C., M. Huet, L. Senegas, B. Milá, C. Thébaud, Y. Bourgeois, A. S. Chaine. 2023. Beyond morphs: genetic and plastic influences on patterns of inter-individual variation in a color polymorphic bird. Journal of Evolutionary Biology, 36(1): 82-94.

Bourgeois, Y., J. Bertrand, B. Delahaie, H. Holota, C. Thébaud*, B. Milá*. 2020. Local adaptation and sexual selection drive intra-island diversification in a songbird lineage: differential divergence in autosomes and sex chromosomes. Molecular Ecology, 29:1137–1153. *: senior co-authors.

Gabrielli M., B. Nabholz, T. Leroy, B. Milá*, C. Thébaud*. 2020. Within-island diversification in a passerine bird. Proceedings of the Royal Society B: Biological Sciences, 287:20192999. *: senior co-authors.

Delahaie, B., J. Cornuault, C. Masson, J. A. M. Bertrand, Y. X. C. Bourgeois, B. Milá*, C. Thébaud*. 2017. Narrow hybrid zones in spite of very low population differentiation in neutral markers in an island bird species complex. Journal of Evolutionary Biology, In press. *: senior co-authors.

Bourgeois, Y. X. C., B. Delahaie, M. Gautier, E. Lhuillier, P.-J. G. Malé, J. A.M. Bertrand, J. Cornuault, K. Wakamatsu, O. Bouchez, C. Mould, J. Bruxaux, H. Holota, B. Milá*, C. Thébaud*. 2017. A novel locus on chromosome 1 underlies the evolution of a melanic plumage polymorphism in a wild songbird. Royal Society Open Science, 4(2):160805. *: senior co-authors.

Bourgeois, Y. X. C., J. A. M. Bertrand, B. Delahaie, J. Cornuault, T. Duval, B. Milá*, C. Thébaud*. 2016. Candidate gene analysis suggests untapped genetic complexity in melanin-based pigmentation in birds. Journal of Heredity, 2016:327-335.  *: senior co-authors

Bertrand, J. A. M., B. Delahaie, Y. X. C. Bourgeois, T. Duval, R. García-Jiménez, J. Cornuault, B. Pujol, C. Thébaud, B. Milá. 2016. The role of selection and historical factors in driving population differentiation along an elevational gradient in an island passerine bird. Journal of Evolutionary Biology, 29:824-836.

Cornuault, J., B. Delahaie, J.A.M. Bertrand, Y.X.C. Bourgeois, B. Milá, P. Heeb, C. Thébaud. 2015. Morphological and plumage colour variation in the Réunion grey white-eye (Aves: Zosterops borbonicus): assessing the role of selection. Biological Journal of the Linnean Society, 114(2):459-473.

Bertrand, J. A. M., Y. X. Bourgeois, B. Delahaie, T. Duval, R. García-Jiménez, J. Cornuault, P. Heeb, B. Milá, B. Pujol, C. Thébaud. 2014. Extremely reduced dispersal and gene flow in an island bird. Heredity, 112:190-196.

Cornuault, J., J. Bertrand, B. Warren, B. Milá, C. Thébaud, P. Heeb. 2013. Timing and number of colonizations but not diversification rates affect diversity patterns in hemosporidian lineages on a remote oceanic archipelago. American Naturalist, 182:820-833.

Bourgeois, Y. X. C., E. Lhuillier, T. Cézard, J. A. M. Bertrand, B. Delahaie, J. Cornuault, T. Duval, O. Bouchez, B. Milá, C. Thébaud. 2013. Mass production of SNP markers in a nonmodel passerine bird through RAD sequencing and contig mapping to the zebra finch genome. Molecular Ecology Resources, 13(5):899-907.

Cornuault, J., A. Khimoun, R. J. Harrigan, Y. Bourgeois, B. Milá, C. Thébaud, P. Heeb. 2013. The role of ecology in the geographical separation of blood parasites infecting an insular bird. Journal of Biogeography, 40(7):1313-1323.

Bourgeois, Y., J. A.M. Bertrand, C. Thébaud, B. Milá. 2012. Investigating the role of the Melanocortin-1 receptor gene in an extreme case of microgeographical variation in the pattern of melanin-based plumage pigmentation. PLOS ONE, 7(12):e50906.

Cornuault, J., A. Bataillard, B. Warren, A. Lootvoet, P. Mirleau, T. Duval, B. Milá, C. Thébaud, P. Heeb. 2012. The role of immigration and in-situ radiation in explaining blood parasite assemblages in an island bird clade. Molecular Ecology, 21:1438-1452.

Bertrand, J. A. M., R. García-Jiménez, Y. Bourgeois, T. Duval, P. Heeb, C. Thébaud, B. Milá. 2012. Isolation and characterization of twelve polymorphic microsatellite loci for investigating an extreme case of microgeographical variation in an island bird (Zosteropsborbonicus). Conservation Genetics Resources, 4(2):323-326.

Milá, B., B. H. Warren, P. Heeb, C. Thébaud. 2010. The geographic scale of diversification on islands: genetic and morphological divergence at a very small spatial scale in the Mascarene grey white-eye (Aves: Zosteropsborbonicus). BMC Evolutionary Biology, 10:158.

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