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.2015 Jun 5;10(6):e0127575.
doi: 10.1371/journal.pone.0127575. eCollection 2015.

Genetic Evidence of Hybridization between the Endangered Native Species Iguana delicatissima and the Invasive Iguana iguana (Reptilia, Iguanidae) in the Lesser Antilles: Management Implications

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Genetic Evidence of Hybridization between the Endangered Native Species Iguana delicatissima and the Invasive Iguana iguana (Reptilia, Iguanidae) in the Lesser Antilles: Management Implications

Barbara Vuillaume et al. PLoS One..

Abstract

The worldwide increase of hybridization in different groups is thought to have become more important with the loss of isolating barriers and the introduction of invasive species. This phenomenon could result in the extinction of endemic species. This study aims at investigating the hybridization dynamics between the endemic and threatened Lesser Antillean iguana (Iguana delicatissima) and the invasive common green iguana (Iguana iguana) in the Lesser Antilles, as well as assessing the impact of interspecific hybridization on the decline of I. delicatissima. 59 I. delicatissima (5 localities), 47 I. iguana (12 localities) and 27 hybrids (5 localities), who were all identified based on morphological characters, have been genotyped at 15 microsatellites markers. We also sequenced hybrids using ND4 mitochondrial loci to further investigate mitochondrial introgression. The genetic clustering of species and hybrid genetic assignment were performed using a comparative approach, through the implementation of a Discriminant Analysis of Principal Component (DAPC) based on statistics, as well as genetic clustering approaches based on the genetic models of several populations (Structure, NewHybrids and HIest), in order to get full characterization of hybridization patterns and introgression dynamics across the islands. The iguanas identified as hybrids in the wild, thanks to morphological analysis, were all genetically F1, F2, or backcrosses. A high proportion of individuals were also the result of a longer-term admixture. The absence of reproductive barriers between species leads to hybridization when species are in contact. Yet morphological and behavioral differences between species could explain why males I. iguana may dominate I. delicatissima, thus resulting in short-term species displacement and extinction by hybridization and recurrent introgression from I. iguana toward I. delicatissima. As a consequence, I. delicatissima gets eliminated through introgression, as observed in recent population history over several islands. These results have profound implications for species management of the endangered I. delicatissima and practical conservation recommendations are being discussed in the light of these findings.

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Conflict of interest statement

Competing Interests:BV is a student of Laboratoire Genindexe. There are no patents, products in development or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

Figures

Fig 1
Fig 1. Main head morphological differences between the two species.
Morphological characterisation of the head ofIguana iguana (Fort Saint-Louis, Martinique). 1. Subtympanic plate. 2. Lower sublabial scales forming a mosaic. 3. Flat sub-labial and labials. 3’. No row of oval scales between the labials and sub-labials. 4. Dewlap edges forming nearly a right angle. 5. Gular spikes extending into the lower half of the dewlap. 6. Gular spikes > 10. 7. Triangular gular spikes. 8. Top of head flat. 9. Eye chestnut brown. 10. Nuchal tubercles. 11. Body colour greenish grey. 12. High dorsal crest scales. Morphological characterization of the headIguana delicatissima (St. Barth). 1.No subtympanic plate. 2. Sublabial row of scales ± parallel to the labial scales. 3. Rounded scales. 3’. Row of oval scales between the labials and sub-labials. 4. Rounded dewlap edge. 5. Gular spikes on the straight upper edge of the dewlap. 6. Gular spikes <7–8. 7. Conical, long and more or less curved gular spikes. 8. Top of head bumpy. 8’. Occipital bumps. 9. Grey eye. 10. Lack of nuchal tubercles. 11. Body colour brownish-grey. 12. Moderately high dorsal crest scales.
Fig 2
Fig 2. Maps of the distribution of the two iguana species in Lesser Antilles.
The left map represents the historical distribution of the species as far it was in the Sixties. The right map is the today distribution.Iguana iguana? represents local populations of uncertain status which are morphologically distinct from continental iguanas (Breuil, 2013). Since then seven main islands lost theirIguana delicatisisma between the Sixties and the Nineties. The dates in green indicate when the allochthonousI.iguana from South and Central America arrived. For Guadeloupe Bank,C indicates the locality of Cluny,A the locality of Anse à Sable,CL the locality of Carangaise-Longueteau andSF the locality of Saint-François. All these latter localities are inhabited by hybrid populations whereI.iguana,I.delicatissima and hybrids are still present.
Fig 3
Fig 3. Photos of different categories of hybrids.
Hybrid (Basse-Terre, Guadeloupe) (IGH 49): probability backcrossdelicatissima, 0.98; probability F2, 0.02 (a) Hybrid (Grande-Terre, Guadeloupe) (IGH 39): probability F2, 0.99; probability backcrossdelicatissima, 0.01(b). Hybrid Grande-Terre (Guadeloupe) (IGH 9): probability F1, 0.80; probability F2, 0.06; probability backcrossdelicatissima, 0.07; probability backcrossiguana, 0.07. (c) Hybrid Grande-Terre (Guadeloupe) (IGH 43): probability backcrossiguana, 0.86; probabilityiguana 0.14 (d). Hybrid (Basse-Terre, Guadeloupe) (IGH 48): probability F2, 0.60; probability backcrossdelicatissima, 0.40 (e). Hybrid (Basse-Terre, Guadeloupe) (IGH 44): probability backcrossdelicatissima, 0.83; probability F2, 0.17 (f).
Fig 4
Fig 4. Species genetic clustering using Structure assuming two genetic clusters k = 2 (a), and hybrids assignment performed with HewHybrids (b) and HIest (c) for individuals morpholocally identified asI.delicatissima,I.iguana or hybrids.
Each vertical bar represent an individual with the color indicating the membership probability to belong either to one of the two genetic cluster (a) or to one of the species or hybrid class (b and c):I.delicatissima (red),I.iguana (green), F1 (blue), F2 (magenta),I.delicatissima backcross (brown),I.iguana backcross (dark green), and for unclassified individuals resulting from the HIest analysis (c): later generation more complex hybrids (grey) and unconfident assignment (white).
Fig 5
Fig 5. Sample space of hybrid genomic proportions.
Distributions of ancestry (S) and individual heterozygosity (Hi) on a bivariate coordinate system for all individuals according to their classification in HIest (a) and individuals assigned as hybrids only (b) identified by their population of origin.
Fig 6
Fig 6. Discriminant analysis of principal component (DAPC).
(a) Bayesian Information Criterion value for a range of number of cluster (K) allowed unambiguous inference of the most likely number of clusters K = 10. (b) Neighbor-joining tree computed on the DAPC distances representing the genetic relationship between the inferred 10 clusters. (c) Visualization of the location of the individuals (points) and clusters (ellipses) in the first two axes of the DAPC space (horizontal: axis 1, vertical: axis 2); a minimum spanning tree linking the two closest clusters in the entire DAPC space are represented by a grey line. (d) Distribution of the number of individual assigned to each cluster across species and hybrids. (e) Bar plot representation the individual assignment to clusters together with their species identity and population of origin.
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References

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Financial support of the project was provided by the Directions régionales de l’Environnement et du Logement de Martinique et de Guadeloupe and by the Natural Reserve of Saint-Barthélemy. Laboratoire Genindexe provided support in the form of salaries for author BV, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of the authors are articulated in the ‘author contributions’ section.

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