In combination with the microsatellite data, our mitochondrial findings are consistent with there being one species of Philornis on
the islands from which we sampled. A population bottleneck was detected
in the entire sample of individuals from the three islands, which is
consistent with the pattern expected from an invasive, recently
colonised species [4-6]. We report low genetic differentiation between island populations of the invasive avian parasite P. downsi on
the Galápagos archipelago. Fly populations on Santa Cruz, Floreana, and
Isabela showed strong evidence for high inter-island gene flow.
However, low levels of divergence were detected between individuals
from Floreana Island and those from Santa Cruz and Isabela when
incorporating geographic sampling information. The molecular variance
was mainly explained at the level of individuals, and not by island,
which further demonstrates the low genetic differentiation between
islands. Bayesian clustering analysis with geographic data assigned
individuals to two genetic clusters, one comprising individuals from
Santa Cruz and Isabela, and the second comprising all individuals from
Floreana Island (Table 3, Figure 4). This might indicate that gene flow in P. downsi between
Floreana and the other islands is restricted to some extent, or that
this island underwent a distinct founding process. Pairwise Fst
between the three islands further indicated that flies on Floreana may
be slightly genetically divergent from flies on the other two islands.
The Bayesian clustering method implemented in STRUCTURE
is considered to be best able to infer correct individual assignments
when genetic differentiation between populations is well defined [48].
Furthermore, the ability to distinguish the source of an individual
decreases under conditions of high dispersal and associated low genetic
differentiation [51,55]. The level of genetic differentiation (Fst) between populations is found to be a useful predictor of the performance of assignment methods [55]. In the current study, the inability of STRUCTURE
to confidently assign individuals to any cluster with certainty may
reflect the lack of power to do so due to the low genetic
differentiation (i.e. Fst) between sampling locations. Thus,
we conclude there was an insufficient signal in the data to confidently
assign individuals under the model of Pritchard et al. [48],
despite reasonably high PI values across loci. Our results are
therefore testament that taking the spatial context of individuals into
account improved the efficiency of our analysis, as found by Fontaine
et al. [53]. Verifying the usefulness of STRUCTURE
to assign individuals correctly where genetic differentiation is low
and dispersal is common requires further study using empirical field
data [51,55].
The current study lacks genetic data from mainland P. downsi populations and data from all islands of the Galápagos where P. downsi occurs,
which will be necessary for a detailed examination of founder effects,
bottlenecks, introduction events and colonisation pathways. Thus,
without knowing where P. downsi populations originally came
from, or where they most recently arrived on the Galápagos archipelago,
a comprehensive invasion history can not be constructed on a
demographic or evolutionary scale [11,56]. However, our findings lay the foundation for a more thorough understanding of the process of P. downsi invasion on the Galápagos archipelago. It is possible that P. downsi arrived on Ecuadorian cargo ships that were transporting fruit to the islands for human consumption [57,58], while it is also suggested that the fly came with imported pigeons (discussed in [59]).
Strong winds and air currents present during El Niño events on the
Galápagos are believed to contribute to insect dispersal between
islands [60],
while transport of humans and materials is also suspected to aid
inter-island insect dispersal. In four other invasive insect species,
the dates of colonisation on each island suggest a wind-mediated
southeast to northwest direction of colonisation across the islands [57]. Such patterns remain unexplored for P. downsi.
Invasion processes
Recently colonised invaders are often subject to a reduction in
genetic variation and population bottlenecks because populations are
not in genetic equilibrium [4-6]. We provide evidence for a population bottleneck in P. downsi across
the three islands examined, which could be due to a small founding
population, low immigration rates, or few introduction events [6,61]. The low allelic diversity across loci and population bottleneck in P. downsi is
further evidence for a small effective population size upon initial
colonisation. However, the occurrence of multiple introductions can not
be excluded, particularly in the absence of comparisons with potential
source populations (e.g. from Ecuador, Trinidad, or Brazil) [13]. Despite the presence of a population bottleneck and the (most likely related) low genetic diversity in P. downsi, the fly has clearly succeeded at establishing and spreading itself across the archipelago in high numbers.
Recently established species may persist at low and possibly
undetectable numbers before becoming noticeably abundant and invasive
years or decades later [5], which may reflect the lag time (i.e. the time between arrival and spread) observed in many species that become invasive [62]. This scenario seems likely concerning the invasion of P. downsi on Galápagos because the fly was not detected in finch nests and identified until 1997 [63], despite the recent discovery of specimens found in collections made in 1964 [13,17]. The parasite has since spread successfully and in high numbers across the archipelago (11 of 13 major islands) [59],
indicating that any lag period that took place has passed. Yet it is
unknown how recently each island was colonised and thus, whether
particular island populations are undergoing a lag period that would
favour the success of an immediate eradication effort (discussed in [64]).
Ecological [12,28,59] findings do not support the current existence of a lag period and indicate that P. downsi has spread successfully in at least 12 avian host species on the Galápagos Islands [12,13]. In the current study, we provide evidence that the P. downsi population
on Floreana Island has detectable levels of genetic differentiation
when compared with two other island populations, which might be the
result of a separate introduction event(s) or colonisation pattern. A
wider geographic sample of locations across habitats and islands is
needed to examine this more definitively in combination with a larger
number of highly polymorphic genetic markers. However, it is clear that
P. downsi populations generally have high connectivity between
islands or high shared ancestry, although variation in population
processes (e.g. rates of dispersal, colonisation histories) between
particular islands may allow for low levels of inter-island genetic
differentiation.
Absence of local genetic divergence
Local populations are expected to evolve adaptive differences in response to differing environmental conditions [64]. The lack of genetic structure in P. downsi on the Galápagos archipelago may reflect the estimated short time period since the flies' introduction (~40 years ago) [3]
such that populations have not yet diverged since colonisation. We
document no genetic structure according to habitat type across islands,
which implies high levels of fly dispersal between the two habitats.
Across islands however, differences in host diversity and distribution,
ecological variables, or colonisation history may result in genetic
divergence due to genetic drift, as was evident from the low genetic
differentiation we document on Floreana Island.
Fly populations may show rapid evolution with geographic cline, as shown by Huey et al. [65] who found increased wing length with latitude in Drosophila subobscura,
just two decades after its introduction into North America. The
evidence we present for high gene flow between habitats implies that
morphological variation in P. downsi is unlikely, though
other insect species on Galápagos show morphological variation and
genetic differentiation between habitats and islands of the archipelago
[56,66,67]. Clinal variation in morphology (and evidence for low dispersal) was also found for Bulimilus land snails on Galápagos [68] and Darwin's small ground finch [26].
Implications for control: the sterile insect technique (SIT)
The use of SIT to control P. downsi on the Galápagos
Islands is perhaps the most appropriate method for eradicating an
invasive fly within this ecologically fragile island ecosystem. SIT is
a non-disruptive method as it does not introduce toxic or foreign
chemicals into the environment, it is species specific, and does not
introduce new genetic material into populations because the released
organisms are not self-replicating [19,69].
The effectiveness of SIT is affected by population genetic
differentiation within the target species because the occurrence of
undetected sub-species or strain differentiation across geographic
populations can be detrimental to widespread sterile male release [19].
Reinfestation of parasitic flies in SIT treated regions have been
explained by genetic differentiation in the target species among
allopatrically separated populations that may be experiencing
reproductive isolation [e.g. [70]].
It is therefore of great advantage to use molecular genetic techniques
for species characterisation and to examine population genetic
structure prior to establishing large-scale sterile male release
programs. We show that gene flow in P. downsi within and
between three islands of the Galápagos is high, and unlikely to result
in reproductive isolation. Thus, release of a single sterile strain of P. downsi could effectively suppress and eradicate the fly across the archipelago. Captive breeding experiments of adult P. downsi from multiple island populations are necessary to determine this with high confidence.
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