INTRODUCTION
Local adaptation of populations to low-quality habitats, such as species
range edges, is crucial for within-species genetic diversity and range
expansion/contraction dynamics, with consequences for long-term species
persistence (Wright 1943; Pulliam 1988; Venail et al. 2008;
Edelaar & Bolnick 2012). The typically asymmetric migration between
core and edge habitats (source-sink dynamics) can play a crucial role in
local adaptation to the latter. Immigrants into the edge populations may
fuel local adaptation by supplementing genetic variation (Holt et
al. 2004; Perron et al. 2007), or retard it by competing with
the locally adapted genotypes or disrupting locally adaptive alleles via
recombination (Figure 1a, 1b) (García-Ramos & Kirkpatrick 1997; Fedorkaet al. 2012; Eriksson & Rafajlović 2021). Theory suggests that
the net effect of immigration on local adaptation will depend on a
number of factors including migration rate; and both positive and
negative effects have been reported in previous empirical studies
(Perron et al. 2007, 2010; Tigano & Friesen 2016; Mirrahimi &
Gandon 2020).
Coevolving natural enemy species have recently been recognized as
important players for population diversification and species
biogeography (Engelkes et al. 2008; Ricklefs 2010; Ricklefs &
Jenkins 2011; Betts et al. 2018). Here we investigate how the
presence of enemy species may limit abiotic adaptation in edge habitats
with and without source-sink dynamics. In an isolated edge habitat,
enemy species can reduce victim population sizes and thus the supply of
genetic variation and the efficiency of natural selection (Hudsonet al. 1998; Bohannan & Lenski 2000); and may also drive the
evolution of defenses that trade-off with growth traits underlying
abiotic adaptation (Figure 1c) (Kraaijeveld & Godfray 1997; Webster &
Woolhouse 1999; Brockhurst et al. 2004; Agrawal et al.2010).
When the enemy species are far more mobile than the victim (as in many
predator-prey and plant-herbivore systems), immigration of the enemy
individuals from the core habitats would further reduce victim
population size, particularly when the core habitats also function as
evolutionary hotspots that promote enemy-victim arms race coevolution
(Figure 1d) (Hochberg & Van Baalen 1998; Lopez Pascua et al.2012; Gorter et al. 2016). This negative effect of the source
populations on the sink populations is an example of enemy-mediated
intraspecific apparent competition (Holt 1977; Morris et al.2004; Ricklefs 2010; Allen et al. 2018). Enemy migration may also
coincide with victim migration, particularly in host-parasite systems.
Here, the net effect for abiotic local adaptation is less predictable:
Immigration of victim species itself may promote local adaptation by
increasing genetic variation, but it is equally possible that the
co-occurring enemy-victim migration leads to repeated sweeps of sink
populations by immigrants and thus prevents local adaptation (Figure 1e)
(Zhang & Buckling 2016; Poulin & de Angeli Dutra 2021). Some more
complex but less realistic scenarios are not considered here, e.g. enemy
species being present in the core, but not edge habitats; or enemy
species having much lower migration rate than victim species.
Here we experimentally test the above hypotheses using a model
bacterium-phage system, Pseudomonas fluorescens SBW25 and its
lytic phage SBW25Φ2 (Buckling & Rainey 2002). This is a host-parasitoid
system as the phages both develop within the bacterial cells and kill
the bacterial cells after replication (Lenski 1984; Buckling & Rainey
2002; Forde et al. 2004). Therefore, the bacterium and the phage
are victim and enemy species, respectively. Due to the experimental
amenability of this system, we are able to study all the five scenarios
illustrated above (Figure 1). We considered a low temperature
environment as an edge habitat for the bacterium and an optimal
temperature its core habitat.