Abstract
BackgroundA controversial topic in evolutionary developmental biology is whether morphological diversification in natural populations can be driven by expansions and contractions of amino acid repeats in proteins. To promote adaptation, selection on protein length variation must overcome deleterious effects of multiple correlated traits (pleiotropy). Thus far, systems that demonstrate this capacity include only ancient or artificial morphological diversifications. The Hawaiian Islands, with their linear geological sequence, present a unique environment to study recent, natural radiations. We have focused our research on the Hawaiian endemic mints (Lamiaceae), a large and diverse lineage with paradoxically low genetic variation, in order to test whether a direct relationship between coding-sequence repeat diversity and morphological change can be observed in an actively evolving system.ResultsHere we show that in the Hawaiian mints, extensive polyglutamine (CAG codon repeat) polymorphism within a homolog of the pleiotropic flowering time protein and abscisic acid receptor FCA tracks the natural environmental cline of the island chain, consequent with island age, across a period of 5 million years. CAG expansions, perhaps following their natural tendency to elongate, are more frequent in colonists of recently-formed, nutrient-rich islands than in their forebears on older, nutrient-poor islands. Values for several quantitative morphological variables related to reproductive investment, known from Arabidopsis fca mutant studies, weakly though positively correlate with increasing glutamine tract length. Together with protein modeling of FCA, which indicates that longer polyglutamine tracts could induce suboptimally mobile functional domains, we suggest that CAG expansions may form slightly deleterious alleles (with respect to protein function) that become fixed in founder populations.ConclusionIn the Hawaiian mint FCA system, we infer that contraction of slightly deleterious CAG repeats occurred because of competition for resources along the natural environmental cline of the island chain. The observed geographical structure of FCA variation and its correlation with morphologies expected from Arabidopsis mutant studies may indicate that developmental pleiotropy played a role in the diversification of the mints. This discovery is important in that it concurs with other suggestions that repetitive amino acid motifs might provide a mechanism for driving morphological evolution, and that variation at such motifs might permit rapid tuning to environmental change.
Highlights
A controversial topic in evolutionary developmental biology is whether morphological diversification in natural populations can be driven by expansions and contractions of amino acid repeats in proteins
The polyglutamine tract in FCA-like proteins varies in length Before extensive experimentation with the mints, we investigated the organismic distribution of the polyQ tract by surveying databases for FCA homologs
The Hawaiian mint FCA-like system suggests the possibility that polyQ variation, as readily measured over a relatively short geological time sequence, contributed to morphological change and participated in incipient speciation
Summary
A controversial topic in evolutionary developmental biology is whether morphological diversification in natural populations can be driven by expansions and contractions of amino acid repeats in proteins. They originated from polyploid (likely octoploid) North American ancestors and diversified from a single introduction to the Hawaiian Islands [13,14] Their morphological and ecological variation is extensive; plants range from subalpine vines to rainforest shrubs, flowers may have either bird or insect pollinated anatomies, and seed dispersal patterns may depend on either dry or fleshy fruits [15]. In contrast to this extensive diversity, genetic variation in nuclear and chloroplast DNA sequence markers has been found to be remarkably low, resulting in a lack of phylogenetic resolution among representatives of the two largest genera, Phyllostegia and Stenogyne [13]
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