Footprints of historical admixture
Despite the aforementioned distributional shifts of host species
resulting from Quaternary climate dynamics, population genetic analyses
revealed evidence for gene flow among Chacoan (Central lineage) and
North Pampean (East lineage) populations of C. cactorum . In
particular, extensive nuclear admixture and sharing of mtDNA haplotypes
occurred across those populations located along the contact area between
northern Pampa and Chaco (Figure 2). This area coincides with a
transition between Chaco and Pampa environments, referred to as the
Espinal (Bucher, 1982). Historical secondary contact among previously
isolated Central and East populations, likely prompted by post glacialOpuntia host range expansion, provides a plausible explanation
for the observed pattern of genetic admixture. Evidence for admixture
was also detected between populations of East and South lineages, both
distributed within the Pampean and Monte regions. This area has been
reported as a landscape corridor facilitating connectivity between
previously separated populations of the grasshopper species D.
vittatus inhabiting grassland and savanna biomes (Rosetti et al.,
2022). Our results would further emphasize the extensive habitat
connectivity between these regions during the Quaternary. Overall, our
results argue against the idea that the human-driven introduction and
intensive cultivation of O. ficus-indica enable rapid expansion
of C. cactorum , promoting contemporary gene flow among
geographically distant populations.
Landscape genomic
analyses
In agreement with inferences of divergence times among three major
lineages as inferred by coalescent-based demographic modeling, the
landscape genomic analyses revealed that the spatial pattern of
population genetic differentiation was best explained by a Quaternary
landscape scenario representing the distribution of climatically
suitable habitats and predicted ranges of host species during the LGM
(Figure 1 and 3). The influence of historical landscape composition on
the contemporary genomic variation pattern was illustrated by the fact
that weakly differentiated populations were predicted to have had high
habitat connectivity in LGM projections. This is the case of JUJ
(northwestern) and FOG (northeastern) populations
(FST=0.088; Table S6), currently separated by 740 km but
subjected to high levels of past habitat connectivity according to
suitability maps. In contrast, a discontinuous habitat was expected to
promote isolation and, thus, genetic differentiation even between
geographically proximate populations. This would be particularly so forC. cactorum , given its presumably limited dispersal ability
because of their short-lived adult stage (Pettey, 1948; Zimmerman, Moran
& Hoffmann, 2000), and illustrated by the southern populations LPS
(southwestern) and BAP (southeastern) which exhibit one of the highest
FST values (FST=0.389), despite the
relatively limited geographic distance separating them of approximately
290 km. Environmental projections during LGM suggest that dispersal
between LPS and BAP was likely limited due to low environmental
suitability, thus limiting gene flow during glacial periods. Thus, our
results would indicate that environmental tolerance together with
limited dispersal could have interacted with landscape features to
generate population genetic structure (Broquet & Petit, 2009; Sherpa et
al., 2020).
Despite signatures for shifts in host species distributions, which may
have influenced contemporary population genetic structure in C.
cactorum, host species use appeared to be less of a consequential
influence. This is at odds with observations in other insect herbivores
(Forbes et al., 2017; Funk et al., 2006; Poveda-MartÃnez et al., 2020),
but in line with field and laboratory host range studies (Varone et al
2014). In areas where there is more than one Opuntia species,
host use by moths was proportional to host species abundance.
Additionally, multiple choice experiments revealed that female C.
cactorum do not exhibit oviposition preference for Opuntiaspecies. Together, these results suggest that host species is not an
important selective agent for C. cactorum , consistent with
evidence from other generalist herbivores (Vidal & Murphy, 2018; Vidal
et al., 2019).