View Program - 2022 Population, Evolutionary, and Quantitative Genetics Conference

Selection continuously reshapes the genetic and phenotypic composition of populations, yet often adaptive changes are not propagated through time due to e.g. prohibitively high drift or gene flow. Nevertheless, selection may still induce temporary phenotypic divergence at extremely small spatial and short temporal scales. These changes may ultimately be of higher ecological importance than long-term evolutionary trends. Selection on polygenic traits in particular may allow for divergence to occur repeatedly every generation without significant reduction in standing genetic variation.

The teleost Fundulus heteroclitus inhabits salt marsh estuaries characterized by high environmental heterogeneity. Population sizes within a marsh are large (>10K) and panmictic breeding results in negligible genetic structure. Yet individual fish demonstrate high site fidelity to distinct microhabitats e.g. tidal ponds or coastal bays, each exhibiting highly disparate temperature and oxygen regimes.

We tagged/recaptured 2000/200 F. heteroclitus and confirmed residency in two microhabitats: a cooler, oxygenated coastal basin and hotter, anoxic tidal ponds. After common-gardening basin and pond residents we measured several, fitness-related traits; critical thermal maximum, resting metabolic rate, cardiac metabolic rate and aquatic surface respiration (ASR) latency. We found significant phenotypic divergence among basin and pond residents in resting metabolic rate (5%, p=0.02), cardiac metabolic rate (9%, p=0.004) and ASR latency (15%, p=0.007), suggestive of divergent selection.

We further identified >10,000 genome-wide single nucleotide polymorphisms using a genotyping-by-sequencing (GBS) approach. By sampling each microhabitat at two time points within a single generation we determined allele frequency change over time. Few individual SNPs show significant allele frequency changes beyond that expected by random mortality. However, the proportion of SNPs exhibiting i) allele frequency changes and ii) divergence among microhabitats is significantly elevated over the neutral expectation. These patterns are consistent with selection on polygenic traits where minor allele frequency changes at multiple loci of small-effect may cause significant phenotypic shifts.

Despite high gene flow and negligible demography, F. heteroclitus displays surprising phenotypic divergence among microhabitats following common-gardening. This is unlikely due to a plastic response but rather divergent selection on polygenic traits. Given high standing genetic variation and large population sizes, selection may be effective enough to regenerate phenotypic divergence repeatedly every generation. While this does not cause any long-term evolutionary change, such temporary phenotypic heterogeneity may be of high ecological importance.

Relentless Selection: Trait divergence under high gene flow