Investigating the role of the Melanocortin-1 Receptor gene in an extreme case of microgeographical variation in the pattern of melanin-based plumage pigmentation

Received: August 23, 2012; Accepted: October 26, 2012; Published: December 5, 2012The Réunion grey white-eye (Zosterops borbonicus) is a single-island endemic passerine bird that exhibits striking geographically structured melanic polymorphism at a very small spatial scale. We investigated the genetic basis of this color polymorphism by testing whether the melanocortin-1 receptor (MC1R), a gene often involved in natural melanic polymorphism in birds, was associated with the observed plumage variation. Although we found three non-synonymous mutations, we detected no association between MC1R variants and color morphs, and the main amino-acid variant found in the Réunion grey white-eye was also present at high frequency in the Mauritius grey white-eye (Zosterops mauritianus), its sister species which shows no melanic polymorphism. In addition, neutrality tests and analysis of population structure did not reveal any obvious pattern of positive or balancing selection acting on MC1R. Altogether these results indicate that MC1R does not play a role in explaining the melanic variation observed in the Réunion grey white-eye. We propose that other genes such as POMC, Agouti or any other genes involved in pigment synthesis will need to be investigated in future studies if we are to understand how selection shapes complex patterns of melanin-based plumage pigmentation.Peer reviewe

Community assembly on remote islands: a comparison of Hawaiian and Mascarene spiders

International audienceAim Spider communities on oceanic islands are assembled through multiple immigration and/or diversification events. In this study, we use a phylogenetic approach to investigate the role of such processes in shaping current patterns of diversity in Tetragnatha spiders from the Mascarene archipelago and to compare these patterns with those found in the Hawaiian archipelago. Location Mascarene archipelago, south-western Indian Ocean; Hawaiian archipelago, Pacific Ocean. Methods Primary techniques included phylogeny reconstruction (mitochondrial cytochrome c oxidase subunit I; histone H3) with and without time calibration, delimitation of species using the general mixed Yule coalescent (GMYC) model, and testing for the presence of gene flow between geographically separated populations using the model of isolation with migration (IMa). Results The current diversity of Tetragnatha on the Mascarenes has arisen through three independent colonization events with no evidence for in situ diversification. This finding is in stark contrast to the pattern observed in Hawaiʻi where two to four independent colonization events have been followed by two massive in situ diversification episodes leading to at least 38 species in total. Main conclusions While net rates of immigration by Tetragnatha lineages appear relatively similar in the two archipelagos, in situ diversification in Tetragnatha only occurred in Hawaiʻi, possibly associated with the extreme geographical isolation of this archipelago relative to the Mascarene archipelago. Owing to the greater geographical proximity of the Mascarene archipelago to source pools such as Madagascar, it seems likely that the persistence of gene flow between the source and the islands and/or niche pre-emption by other spider lineages may have reduced opportunities for diversification despite an apparently favourable ecological context

Narrow hybrid zones in spite of very low population differentiation in neutral markers in an island bird species complex

Patterns of phenotypic and genic frequencies across hybrid zones provide insight into the origin and evolution of reproductive isolation. The Reunion grey white‐eye, Zosterops borbonicus, exhibits parapatrically distributed plumage colour forms across the lowlands of the small volcanic island of Reunion (Mascarene archipelago). These forms meet and hybridize in regions that are natural barriers to dispersal (rivers, lava fields). Here, we investigated the relationship among patterns of differentiation at neutral genetic (microsatellite) markers, phenotypic traits (morphology and plumage colour) and niche characteristics across three independent hybrid zones. Patterns of phenotypic divergence revealed that these hybrid zones are among the narrowest ever documented in birds. However, the levels of phenotypic divergence stand in stark contrast to the lack of clear population neutral genetic structure between forms. The position of the hybrid zones coincides with different natural physical barriers, yet is not associated with steep changes in vegetation and related climatic variables, and major habitat transitions are shifted from these locations by at least 18 km. This suggests that the hybrid zones are stabilized over natural dispersal barriers, independently of environmental boundaries, and are not associated with niche divergence. A striking feature of these hybrid zones is the very low levels of genetic differentiation in neutral markers between forms, suggesting that phenotypic divergence has a narrow genetic basis and may reflect recent divergence at a few linked genes under strong selection, with a possible role for assortative mating in keeping these forms apart.The first author was supported by a MESR (Ministère de l'Enseignement Supérieur et de la Recherche) PhD scholarship during this study. The work was funded by Agence Française pour le Développement, a National Geographic Society Grant, Fondation pour la Recherche sur la Biodiversité (FRB), the ‘Laboratoire d'Excellence’ TULIP (ANR‐10‐LABX‐41) and the SYNTHESYS Project (http://www.synthesys.info/) which was financed by European Community Research Infrastructure Action under the FP7 ‘Capacities’ Programme at the Museo Nacional de Ciencias Naturales (CSIC) in Madrid, Spain.Peer Reviewe

Map showing <i>Z. borbonicus</i> sampling localities, and distribution of the four morphs on Réunion.

<p>Letters correspond to the different plumage morphs: A: Brown morph; B: Grey morph; C: Grey-headed brown morph; and D: Grey-headed brown-naped brown morph. For a more detailed description of pigmentation phenotypes, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0050906#pone.0050906-Gill1" target="_blank">[17]</a>. Adapted from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0050906#pone.0050906-Hubbard1" target="_blank">[18]</a>.</p

Amino-acids variants observed at the <i>MC1R</i> locus in 51 <i>Z. borbonicus</i> individuals representing the four Réunion morphs and nine <i>Z. mauritianus</i> individuals.

<p>For each variant the corresponding nucleotide substitution is indicated, with its state (heterozygous or homozygous) in each morph and species studied here. Sequences were numbered in reference to the chicken genome (Genbank accession number: AY220305).</p

Diversity statistics and results from selection tests for <i>Z. borbonicus</i> morphs.

<p>Π: nucleotide diversity. S: number of segregating sites. Significance levels:</p>*<p>p<0.05;</p>**<p>p<0.01.</p

Data from: Candidate gene analysis suggests untapped genetic complexity in melanin-based pigmentation in birds

Studies on melanin-based color variation in a context of natural selection have provided a wealth of information on the link between phenotypic and genetic variation. Here, we evaluated associations between melanic plumage patterns and genetic polymorphism in the Réunion grey white-eye (Zosterops borbonicus), a species in which mutations on MC1R do not seem to play any role in explaining melanic variation. This species exhibits five plumage color variants that can be grouped into three color forms which occupy discrete geographic regions in the lowlands of Réunion and a fourth form which comprises two color morphs (grey and brown), occurs at high elevation, and represents a true color polymorphism. We conducted a comprehensive survey of sequence variation in 96 individuals at a series of seven candidate genes other than MC1R that have been previously shown to influence melanin-based color patterns in vertebrates, including genes that have rarely been studied in a wild bird species before: POMC, Agouti, TYR, TYRP1, DCT, Corin and SLC24A5. Of these seven genes, two (Corin and TYRP1) displayed an interesting shift in allele frequencies between lowland and highland forms and a departure from mutation-drift equilibrium consistent with balancing selection in the polymorphic highland form only. Sequence variation at Agouti, a gene frequently involved in melanin-based pigmentation patterning, was not associated with color forms or morphs. Thus, we suggest that functionally important changes in loci other than those classically studied may beare involved in the color polymorphism exhibited by the Réunion grey white-eye and possibly many other non-model species

Localities and number of birds sampled on the islands of Réunion and Mauritius.

<p>Localities and number of birds sampled on the islands of Réunion and Mauritius.</p