Abstract
The paradox of how invasive species cope with novel selective pressures
with limited genetic variation is a fundamental question in molecular
ecology. Several mechanisms have been proposed, but they can lack
generality and predictive power. Here, we introduce an alternative
mechanism, genetic redundancy, wherein changes in multiple combinations
of loci can achieve a fitness optimum for polygenic traits, and thus the
variations left after the founder effect may be sufficient for
adaptation. We tested the potential importance of genetic redundancy in
environmental adaptation of Colorado potato beetle (CPB) in introduced
Eurasia. Population genomic analyses showed substantial genetic
depletion following a single introduction event, which supports invasive
CPB as a classic system for the paradox study. Genome-environment
association analyses revealed a suite of loci and gene functions
plausibly related to cold stress. Notably, a substantial portion of loci
showed different contributions to similar or identical environments.
Such non-parallel evolution indicates their potential redundancy to
overall fitness. Furthermore, one important adaptive gene function,
“phospholipid production”, was represented by more than one
independent linkage cluster, suggesting some gene functional redundancy
in cold resistance. Taken together, these results support the hypothesis
that genetic redundancy can promote the adaptability of polygenic traits
despite strong genetic depletion, thus providing a general mechanism for
resolving the genetic paradox of invasion. More broadly, genetic
redundancy, as an inherent feature of the genome, may have contributed
to the evolutionary success of invasive species in many aspects.