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

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.

Hybridization and extinction

“…; Vuillaume et al. ). While our review focuses on extinction through hybridization, we consider its likelihood in the context of hybridization's many potential outcomes and the conditions that may favor one particular outcome over another.…”

“…These include outcomes that maintain or increase diversity such as stable hybrid zones, the evolutionary rescue of small inbred populations, the origin and transfer of adaptations, the reinforcement of reproductive isolation, and the formation of new hybrid lineages (Anderson 1949;Ellstrand and Schierenbeck 2000;Mallet 2007;Abbott et al 2013;Frankham 2015). Alternatively, hybridization can decrease diversity through the breakdown of reproductive barriers, the merger of previously distinctive evolutionary lineages, and the extinction of populations or species (Rieseberg et al 1989;Ellstrand 1992;Levin et al 1996;Rhymer and Simberloff 1996;Allendorf et al 2001;Buerkle et al 2003;Vuillaume et al 2015). While our review focuses on extinction through hybridization, we consider its likelihood in the context of hybridization's many potential outcomes and the conditions that may favor one particular outcome over another.…”

Conservation genomics in the fight to help the recovery of the critically endangered Siamese crocodile Crocodylus siamensis

“…Small isolated populations are specifically sensitive in this regard as they are more vulnerable to fragmentation and genetic drift leading to increased inbreeding, concomitant loss of genetic diversity and heightened risk of extinction (Allendorf, Hohenlohe, & Luikart, ; Frankham, ; Keller & Waller, ). In many species that have become exceedingly rare, surviving individuals can no longer find mates of their own species and resort to hybridization, leading to a loss of genetic purity (Cabria et al, ; Cordingley et al, ; Gese et al, ; Lancaster, Gemmell, Negro, Goldsworthy, & Sunnucks, ; Pinto, Beja, Ferrand, & Godinho, ; Rheindt & Edwards, ; Schwartz et al, ; Todesco et al, ; Vuillaume, Valette, Lepais, Grandjean, & Breuil, ; Wayne & Shaffer, ).…”

A story of nasal horns: A new species ofIguanaLaurenti, 1768 (Squamata, Iguanidae) in Saint Lucia, St Vincent & the Grenadines, and Grenada (Southern Lesser Antilles) and its implications for the taxonomy of the genusIguana

“…At that time, the central group was known to be present only in Guadeloupe (Les Saintes, Basse-Terre and Grande-Terre). This group is not native and is the descent of invasive common iguanas from French Guiana Breuil 2016; Vuillaume et al 2015). Now, however, alien iguanas from Central and South America are present throughout most of this region (van den Burg et al 2018) except Saint Christopher and Nevis, Dominica, Petite Terre and some satellites of Saint Barthélemy, Anguilla, and Martinique.…”

“…Breuil (2013, 2016) reported that I. iguana was first introduced from French Guiana to Les Saintes in the mid-19 th Century, and Breuil (2009) and Breuil et al (2010) explained how this species arrived on Basse-Terre. The unfortunate result of this introduction of I. iguana has been the elimination of the native I. delicatissima through hybridization and competition from Terre-de-Bas and Terre-de-Haut (Les Saintes) and Grande-Terre, a process that is continuing at present on Basse-Terre (Breuil et al 2010; Vuillaume et al 2015; Breuil 2013, 2016). More recently, Iguana x Cyclura hybrids have been recorded from Little Cayman Island (Moss et al 2017), showing the lack of isolating mechanisms between these Caribbean genera.…”