Introduction
Archipelagos provide unique opportunities for phylogeographic analyses.
They are geographically isolated and dispersal-mediated gene flow among
individual islands is limited for some taxa (Emerson & Hewitt, 2005),
such as terrestrial squamate reptiles. Located in the Tropical Eastern
Pacific 960 km off the coast of Ecuador, the Galápagos archipelago has
long been recognized as a model system for evolutionary and
biogeographic studies (Darwin, 1859; Emerson, 2002; Grant & Grant,
2014; Losos & Ricklefs, 2009; Parent, Caccone, & Petren, 2008).
At present, the Galápagos archipelago includes 123 islands, only 13 of
which are larger than 10 km2 (Snell, Stone, & Snell,
1996). Among the larger islands, Floreana is one of the few inhabited
islands, and lies on the southern limit of the archipelago (Fig. 1).
Only three years before Darwin’s historical arrival to the Galápagos in
1835, the first human colony of the Galápagos was established in
Floreana under the term of Ecuador’s first president, Juan José Flores,
after whom the island was named in Spanish. The new inhabitants
introduced domestic animals, mice and rats, and the domestic animals
established feral populations. Floreana’s terrestrial biodiversity was
thereby impacted; several vertebrate species including Floreana’s giant
tortoise (Chelonoidis niger Quoy & Gaimard, 1824), racer snake
(Pseudalsophis biserialis Günther, 1860) and mockingbird
(Mimus trifasciatus Gould, 1837) went extinct in the following
40-50 years (Broom, 1929; Steadman, 1986). Of these, Floreana’s racer
snake and mockingbird still survive on adjacent islets (Grant, Curry, &
Grant, 2000; Thomas, 1997), such as Champion and Gardner, which lack
introduced mammals. In contrast, the Floreana lava lizardsMicrolophus grayii Bell, 1843 and the Floreana leaf-toed geckosPhyllodactylus baurii Garman, 1892 have survived human impacts
both on Floreana and adjacent islets, although both species are
frequently predated by feral and domestic cats in Floreana (Paula
Castaño pers. obs. 2018; Rodriguez & Fessl, 2016; Steadman 1986). A
population viability analysis of Floreana lava lizards showed that lack
of recruitment was the primary factor restricting population size on
Floreana and suggested that eradication of feral cats and invasive
rodents might have a positive effect (Rodriguez & Fessl, 2016).
Floreana has an area of 173 km2 and is surrounded by
several satellite islets, including Caldwell, Enderby, Champion, Gardner
and Watson. With an estimated age of 1.5–2.3 million years (Geist,
Snell, Snell, Goddard, & Kurz, 2014; White, McBirney, & Duncan, 1993),
Floreana is of intermediate age of islands within the archipelago.
Noting that some Galápagos islands are broadly connected by shallow
seabed, some authors have proposed that Pleistocene changes in sea level
had a strong influence on the evolution of land-locked vertebrates by
allowing contact among populations from different islands during
glaciation periods (Ali & Aitchison, 2014; Geist et al., 2014;
Poulakakis, Russello, Geist, & Caccone, 2012). For example, Fernandina,
Isabela, Pinzón, Rábida, Santiago, Baltra and Santa Fe are connected by
shallow water (<200 m); therefore, these islands were possibly
connected by land bridges during Pleistocene glaciations, when sea level
fell to between -90 and -130 m below the present level, for 5–10 kyr
intervals (Ali & Aitchison, 2014). In contrast, other major islands are
isolated from one another by a deeper (>500 m) ocean floor
and were thus not connected to other large islands in the recent past.
Nonetheless, these islands were presumably connected to satellite islets
separated by depths <200 m. According to this
paleogeographical model, Floreana was connected to the satellite islets
of Caldwell, Champion and Enderby, whereas Gardner and Watson were
separated and formed a single islet during Pleistocene glaciations (Fig.
1; Geist et al., 2014). Consequently, present land organisms with
limited dispersal abilities from Floreana should be more similar
genetically to those from Caldwell, Champion and Enderby than they are
to organisms from Gardner and Watson due to gene flow during Pleistocene
low sea-level periods.
If the paleogeographic model holds true, it has great implications for
the conservation of Floreana’s terrestrial vertebrates. Plans currently
exist to implement an invasive rodent and feral cat eradication program
using a rodenticide bait containing the second-generation anticoagulant
brodifacoum (Island Conservation, 2013). Brodifacoum is highly toxic to
mammals and birds; therefore, it could represent a serious threat for
non-target wildlife species through primary or secondary exposure
pathways (Broome, et al., 2014; Rueda et al., 2016). Fisher, Campbell,
and Castaño (2017) identified that Floreana lava lizards and Floreana
leaf-toed geckos were at low risk (island population may be reduced by
up to 10%) if exposed to brodifacoum, in agreement with a previous
study showing low toxicity of this rodenticide in the fence lizardSceloporus occidentalis (Weir et al., 2015), as well as findings
from previous successful invasive rodent eradications implemented in the
Galápagos Islands (Rueda et al., 2019). However,
However, as both species are endemic to Floreana and are considered
evolutionary significant units (Young, 2016), mitigation actions (e.g.
captive holding in situ or translocation from satellite islets)
should be considered if the invasive rodent and feral cat eradication
program is to be implemented. Thus, knowing the genetic affinities among
lizard populations of Floreana and surrounding islets is of great
importance for their conservation. Moreover, if a future goal is to
recover Floreana’s extirpated endemics using the closest genetic
counterparts, then reintroduction strategies should consider
translocating individuals from islets containing populations recently
(Pleistocene) connected with Floreana.
The aim of this study was to test the hypothesis that haplotypes of
Floreana lava lizards and Floreana leaf-toed geckos from Floreana are
more similar to those from Champion than they are to those from Gardner,
thereby supporting the Pleistocene paleogeographic model. If the
invasive rodent and feral cat eradication program on Floreana Island is
implemented, our results will help identify the most appropriate risk
mitigation action for both lizard species.