DISCUSSION
Migration of individuals from high- to low-quality habitats often help
to maintain population sizes in the latter and may have varying effects
on local adaptation. The high-quality habitats may also support greater
abundances of natural enemies, and the effects of source-sink dynamics
on local adaptation in low-quality habitats might fundamentally be
altered by coevolving enemies. Our study suggests a negative effect of
immigration of coevolving enemies on abiotic local adaptation of
victims, particularly when enemies, but not victims themselves, migrate
from source to sink habitats.
While bacterial evolution lines in a low temperature habitat showed
obvious evolutionary adaptation in terms of population growth
performance, bacterial immigration from an optimal temperature habitat
reduced such adaptation (B versus B+IB microcosms, Figure 3), consistent
with a “swamp by gene flow” view (Bennett & Lenski 2007;
Rodríguez-Verdugo et al. 2014; Micheletti & Storfer 2020). It is
likely that mutational supply was not, or only weakly, limited in our
bacterial populations at 10°C (bottleneck population size >
3 × 107), and immigration had little positive effect
on mutation supply, but affected the fixation of beneficial mutations.
The presence of phages limited abiotic adaptation of bacterial
populations. It is possible that fixation of phage-resistant mutations
may constrain the acquisition of beneficial mutations for abiotic
adaptation (Scanlan et al. 2015). Furthermore, the fact that our
bacterial growth performance may become even poorer than the ancestral
strain (in BP+IP coevolution lines) suggests fitness costs of bacterial
resistance evolution, consistent with earlier studies (Buckling &
Rainey 2002; Brockhurst et al. 2004; Buckling et al.2006). The bacterial growth performance from BP and BP+IBP coevolution
lines was not poorer than the ancestral strain, though no difference in
bacterial resistance to phages was found among the three types of
coevolution lines. This suggests that bacterial adaptation that
compensated for the fitness costs of resistance should have occurred;
and such abiotic adaptation was less efficient in the BP+IP microcosms
(probably due to the much lower bacterial population sizes and thus
lower mutation supply). For the BP+IBP coevolution lines, the bacterial
immigrants per se may have promoted bacteria abiotic adaptation,
contrary to the effect of bacterial immigrants to the B+IB microcosms.
The negative impact of immigrant phages on bacterial sink adaptation is
presumably because the source phages evolved greater infectivity than
sink phages and/or achieved higher densities. While the intensity of
bacteria-phage coevolution, and hence the extent of phage infectivity
evolution, did not differ between our 28 and 10°C microcosms at transfer
20, weak signals of more intense coevolution were detected for the core
microcosms at transfer 8 (Supplementary text; Figure S2). This is
consistent with previous studies: A previous short term (6-transfer)
experiment showed that a modestly low temperature (15°C) could slow
bacteria-phage coevolution compared with a higher temperature (25°C)
(Zhang & Buckling 2016); and a 10-transfer coevolution study across 3
temperatures (8, 17, 28°C) found more intense coevolution at higher
temperatures (Gorter et al. 2016). We suggest that the extremely
low bacterial population sizes of BP+IP microcosms during the early
stage of evolution experiment result from a “mass effect” of phage
immigrations (and higher phage infectivity if coevolution was faster in
28°C microcosms at the early stages), and the low population sizes
limited abiotic adaptation. The persistently lower bacterial population
sizes of BP+IP microcosms compared with BP microcosms at the late stages
of the evolution experiment, however, might be due to the poorer growth
performance as a consequence of limited abiotic adaptation, but not
greater top-down control effect by phages. The top-down control effect
at the end of the evolution experiment could be estimated for BP and
BP+IP microcosms by comparing their population sizes (in the presence of
phages) and the abiotic adaptation measures (in the absence of phages);
and this suggest that phages reduced bacterial population densities by
73% in BP and 62% in BP+IP microcosms (Figure S3).
Migration in coevolving systems often have asymmetric effects on victim
and enemy populations (Gandon et al. 1996; Lion et al.2006). For instance, under homogeneous landscapes, phage Φ2 usually
benefits from migration more than P. fluorescens on a global
scale as phages are more genetically constrained and have a lower
evolutionary potential (Brockhurst et al. 2003, 2007; Morganet al. 2005, 2007). Under heterogeneous landscapes, mixed
evidence was found for the effect of gene flow on the evolution of phage
infectivity (Forde et al. 2004, 2007); and a net beneficial
effect of bacterial immigrations on abiotic adaptation was inferred in
the BP+IBP treatment here. Therefore, how migration affects the
coevolving populations may depend on not only the heterogeneity between
patches, but also the migration pattern of victims and enemies (Gandon
& Michalakis 2002; Tigano & Friesen 2016; Zhang & Buckling 2016).
In summary, by (co)evolving bacteria and phage populations under various
migration regimes across heterogenous environments (Figure 1), we found
that abiotic adaptation of bacteria in sink environment was limited by
the immigrated phages from the source environment. These results
highlight that traditional thinking about source-sink dynamic should be
interpreted with caution in antagonistic coevolution systems; immigrant
victims and enemies may have opposing effects on the abiotic adaptation
of victims in the edge habitats. Future work involving a variety of
stress gradients would determine the generality of these findings, and
therefore help to understand species’ range expansion in nature with
implications for conservation planning (Engelkes et al. 2008;
Benning & Moeller 2021).