Migration load, competition, and metabolic trade-offs shape spatial divergence through eco-evolutionary dynamics

Abstract

Evolutionary models predict that trade-offs related to resource utilization promote local specialization and diversification in spatially heterogeneous environments. However, diversification is also influenced by ecological feedback mechanisms - such as frequency-dependent resource use - and their interaction with migration. To investigate how spatial variation affects diversification, we conducted an evolution experiment exposing populations of Lactococcus cremoris to divergent selection on two carbon sources: fructose and galactose. Using a continuous culture system, we partitioned these resources into two isolated patches (allopatry), two patches with constant migration between them (parapatry), and one fully-mixed patch (sympatry). Resource specialization and subsequent phenotypic diversification evolved in all treatments, revealing a metabolic trade-off between fructose and galactose utilization. Compared to treatments without migration, spatial variation produced a distinctive temporal pattern: migration initially delayed specialization on galactose but later accelerated it. This temporal pattern emerged from eco-evolutionary feedbacks operating through two mechanisms: (i) early in the experiment, higher population density in the better-suited fructose patch increased the influx of maladapted immigrants into the galactose patch, slowing local adaptation; however, (ii) as strains adapted locally to galactose, population density increased in the galactose patch and density asymmetries weakened. Simultaneously, the competitive ability of immigrants declined as residents became increasingly specialized in their local resources, progressively reducing the effective migration rate and allowing accelerated divergence. Our experiment demonstrates how the likelihood and tempo of spatial divergence depend on the evolvability of phenotypic trade-offs and their dynamic interaction with migration load and population density.