Outbreeding depression from physiological refugia limits adaptation of a
native gastropod to an invasive predator
Abstract
Biological invasions have caused the loss of freshwater biodiversity
worldwide. The interplay between adaptive responses and demographic
characteristics is expected to be important for the resilience of
populations to biological invasions, but the interaction between these
factors is poorly understood. The native freshwater gastropod Amnicola
limosa is distributed along spatial variation in impact from an invasive
molluscivorous fish (Neogobius melanostomus), as well as calcium
concentrations, limiting the distribution of this invader (refuges). We
investigated the potential for genetic adaptation of A. limosa to the
invasive predator and the low calcium habitats. We conducted pooled
whole-genome sequencing of twelve gastropod populations from the Upper
St. Lawrence River, complemented with a laboratory reciprocal transplant
of wild F0 A. limosa to measure survival and fecundity in treatments of
water calcium concentration (low/high) and round goby cue
(present/absent). We quantified gene flow between the habitat types to
test how population structure might interact with adaptation. We found
that low calcium, uninvaded habitats could act as refugia for the
gastropods from the invasive fish and provide migrants to declining
invaded gastropod populations through strong gene flow (i.e.,
demographic rescue), which also maintained genetic diversity (i.e.,
genetic rescue). However, we also detected signatures of divergent
selection between habitat types and evidence of low fitness of
individuals from refuge populations in both habitat types. This suggests
that migrants from refuges could introduce maladapted alleles to
recipient populations in high calcium, invaded habitats, thereby
reducing fitness via outbreeding depression and producing conflict
between demographic, genetic, and evolutionary rescue.