Abstract
Understanding the relative importance of reproductive isolating mechanisms across the speciation continuum remains an outstanding challenge in evolutionary biology. Here, we examine a common isolating mechanism, reproductive phenology, between plant sister taxa at different stages of adaptive divergence to gain insight into its relative importance during speciation. We study 17 plant taxa that have independently adapted to inhospitable serpentine soils, and contrast each with a nonserpentine sister taxon to form pairs at either ecotypic or species-level divergence. We use greenhouse-based reciprocal transplants in field soils to quantify how often flowering time (FT) shifts accompany serpentine adaptation, when FT shifts evolve during speciation, and the genetic versus plastic basis of these shifts. We find that genetically based shifts in FT in serpentine-adapted taxa are pervasive regardless of the stage of divergence. Although plasticity increases FT shifts in five of the pairs, the degree of plasticity does not differ when comparing ecotypic versus species-level divergence. FT shifts generally led to significant, but incomplete, reproductive isolation that did not vary in strength by stage of divergence. Our work shows that adaptation to a novel habitat may predictably drive phenological isolation early in the speciation process.
Highlights
A major goal of speciation research is to understand the relative importance of different reproductive isolating mechanisms, both across taxa and at different time points during the speciation process [1,2]
We modelled flowering time (FT) divergence among pairs as a function of a fixed intercept (β2) that indicates the average magnitude of shifts in tolerator sister taxa pairs, a random intercept that accounts for phylogenetic relatedness among pairs (β0), a fixed effect for pair type that indicates how different the average shift in endemic pairs is relative to tolerator pairs (β1), and a fixed effect for year the pair was grown in the greenhouse (β3)
We used phylogenetic generalized least squares (PGLS) models to test for differences in phenological isolation between endemic and tolerator pairs in two ecological contexts: (i) when sister taxa are in their home soils and (ii) when sister taxa are in a common nonserpentine soil
Summary
A major goal of speciation research is to understand the relative importance of different reproductive isolating mechanisms, both across taxa and at different time points during the speciation process [1,2]. Selection can make initially plastic reproductive isolation permanent through canalization if the plasticity is adaptive or reduce it through countergradient selection if the plasticity is a maladaptive stress-mediated response to a marginal habitat [21] These multiple processes all lead to the prediction that reproductive isolation will be more strongly genetically based than plastic for taxa further along the speciation continuum. Understanding the importance of phenological isolation at different stages in the speciation process requires understanding how often, at what stage, and to what degree genetically based versus plastic changes in phenology evolve following ecological divergence. We use a greenhouse-based reciprocal transplant experiment in field-collected soil to quantify genetic and plastic differences in both flowering onset—hereafter referred to as FT—and overall phenological isolation within each sister taxa pair (figure 1b–d). We use phenotypic selection analyses in serpentine soil to ask whether plastic shifts in serpentine soil are adaptive or maladaptive, and to assess whether plasticity in serpentine taxa evolved following colonization of serpentine
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