Adaptation in temporally variable environments: stickleback armor in periodically breaching bar‐built estuaries

Abstract

The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar-built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re-form within a few weeks or months, thereby re-isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within-population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes Eda and Pitx1 and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among-population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within-population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype and the presence of predators, thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within-population variation while reducing, but not eliminating, among-population variation driven by spatial environmental variation.

Ionome and elemental transport kinetics shaped by parallel evolution in threespine stickleback

“…Variation at the Eda locus has previously been shown to influence N:P ratio, with low‐plated individuals having higher N:P, and plate phenotype is a significant predictor of %P in stickleback both within polymorphic populations and across populations (Durston & El‐Sabaawi ; Paccard et al . ). Here we use a population with a stable polymorphism at the Eda locus that shows no evidence of population structure linked to Eda genotype (Marchinko et al .…”

“…Our results suggest that the effects of the Eda locus manifest differences in the content of trace elements, more so than in P and Ca (Durston & El‐Sabaawi ; Paccard et al . ), but that life history differences found between Eda genotypes in nature obscure these effects.…”

“…; Paccard et al . ) and that armour phenotypes can influence nutrient excretion (El‐Sabaawi et al . ).…”

The combined use of raw and phylogenetically independent methods of outlier detection uncovers genome‐wide dynamics of local adaptation in a lizard

“…This is remarkable for a terrestrial vertebrate with limited dispersal ability (Santos et al, 2008) after 3 millions of years of lineage divergence (Carranza et al, 2006). At the same time, the combination of divergence subject to selection, maintenance of ancestral adaptive variation, and permeability to gene flow may have rendered the large Psammodromus a species able to adapt to a wide variety of habitats (Lande & Shannon, 2006;Mackay, 1981;Paccard et al, 2018;Parter et al, 2008;Peniston et al, 2019;Welch & Jiggins, 2014), a trait which may underlie its success as the most abundant and widespread Iberian lizard (Huang et al, 2016;Pleguezuelos, Marquez, & Lizana, 2004 Levinst, 1962). After all, if only one dimension of environmental variation is considered, moving away from one end of the gradient inevitably leads to approaching the other end (Lahti et al, 2009).…”

“…This source of ancestral genetic variation should be detected by ROA in the form of divergent outliers with high levels of homozygosity in populations at the extremes of the phenotypic (and environmental) gradient, but with higher than average heterozygosity in the Lerma population. If this was the case, adaptive genetic variation would predate lineage splitting, when it could be either neutral, adaptive to an intermediate environment or maintained by adaptation to a geographically unstructured environmental heterogeneity (Huang, Tran, & Agrawal, ; Mackay, ; McDonald & Ayala, ; Paccard et al, ; Parter, Kashtan, & Alon, ; Welch & Jiggins, ). This variation would be divergently selected in the different ecological scenarios occupied by where eastern and western lineages (Díaz et al, ).…”