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Maintenance of Adaptive Dynamics and No Detectable Load in a Range-Edge Outcrossing Plant Population.

ABSTRACT: During range expansion, edge populations are expected to face increased genetic drift, which in turn can alter and potentially compromise adaptive dynamics, preventing the removal of deleterious mutations and slowing down adaptation. Here, we contrast populations of the European subspecies Arabidopsis lyrata ssp. petraea, which expanded its Northern range after the last glaciation. We document a sharp decline in effective population size in the range-edge population and observe that nonsynonymous variants segregate at higher frequencies. We detect a 4.9% excess of derived nonsynonymous variants per individual in the range-edge population, suggesting an increase of the genomic burden of deleterious mutations. Inference of the fitness effects of mutations and modeling of allele frequencies under the explicit demographic history of each population predicts a depletion of rare deleterious variants in the range-edge population, but an enrichment for fixed ones, consistent with the bottleneck effect. However, the demographic history of the range-edge population predicts a small net decrease in per-individual fitness. Consistent with this prediction, the range-edge population is not impaired in its growth and survival measured in a common garden experiment. We further observe that the allelic diversity at the self-incompatibility locus, which ensures strict outcrossing and evolves under negative frequency-dependent selection, has remained unchanged. Genomic footprints indicative of selective sweeps are broader in the Northern population but not less frequent. We conclude that the outcrossing species A. lyrata ssp. petraea shows a strong resilience to the effect of range expansion.

SUBMITTER: Takou M

PROVIDER: S-EPMC8097302 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundOutcrossing between populations can exert either positive or negative effects on offspring fitness. Cyclically parthenogenetic rotifers, like other continental zooplankters, show high genetic differentiation despite their high potential for passive dispersal. Within this context, the effects of outcrossing may be relevant in modulating gene flow between populations through selection for or against interpopulation hybrids. Nevertheless, these effects remain practically unexplored in rotifers. Here, the consequences of outcrossing on the rotifer Brachionus plicatilis were investigated. Cross-mating experiments were performed between a reference population and three alternative populations that differed in their genetic distance with regard to the former. Two offspring generations were obtained: F1 and BC ('backcross'). Fitness of the outcrossed offspring was compared with fitness of the offspring of the reference population for both generations and for three different between-population combinations. Four fitness components were measured throughout the rotifer life cycle: the diapausing egg-hatching proportion, clone viability (for the clones originating from diapausing eggs), initial net growth rate R for each viable clone, and the proportion of male-producing clones. Additionally, both the parental fertilisation proportion and a compound fitness measure, integrating the complete life cycle, were estimated.ResultsIn the F1 generation, hybrid vigour was detected for the diapausing egg-hatching proportion, while R was lower in the outcrossed offspring than in the offspring of the reference population. Despite these contrasting results, hybrid vigour was globally observed for the compound measure of fitness. Moreover, there was evidence that this vigour could increase with the genetic differentiation of the outcrossed populations. In the BC generation, the hybrid vigour detected for the egg-hatching proportion in the F1 generation reverted to outbreeding depression. By contrast, signs of hybrid vigour were observed for clone viability and R. The opposing trends observed for different life-cycle stages yielded a global pattern of hybrid vigour in the BC generation for two out of the three between-population comparisons.ConclusionsResults suggest that outbreeding depression does not constitute a barrier to gene flow. In newly-founded populations, where the population size is still small, dilution of immigrants should be low. Thus, a lack of outbreeding depression would allow gene flow to have an impact on the genetic composition of these populations.

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Maintenance of Adaptive Dynamics and No Detectable Load in a Range-Edge Outcrossing Plant Population.

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