Heterogeneous Selection on LEGCYC Paralogs in Relation to Flower Morphology and the Phylogeny of Lupinus (Leguminosae)

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An analysis of the molecular evolution of two LEGCYC paralogs in Lupinus (Genisteae: Leguminosae) reveals a varied history of site-specific and lineage-specific evolutionary rates and selection both within and between loci. LEGCYC genes are homologous to regulatory loci known to control floral symmetry and adaxial flower organ identity in Antirrhinum and its relatives. Within Lupinus, L. densiflorus is unusual in having flowers with a proportionally smaller standard (fused adaxial petals) and larger wings (lateral petals) than other lupin species. Phylogenetic estimates of the nonsynonymous/synonymous substitution rate ratio, ω, suggest that along the L. densiflorus lineage, positive selection ( > 1) acted at some codon sites of one paralog, LEGCYC1B, and greater purifying selection ( < 1) acted at some sites of the other paralog, LEGCYC1A. Overall, LEGCYC1A appears to be evolving faster than LEGCYC1B, and both paralogs are evolving faster than the internal transcribed spacer (ITS) region of nr DNA. The predominant historical pattern inferred is a highly heterogeneous “selectional mosaic” which we suggest may be typical of the teosinte branched 1-cycloidea-PCF (TCP) class of transcriptional activators, and possibly other genes. Codon models that do not account for both site-specific and lineage-specific variation in ω do not detect positive selection at these loci. We suggest a modification of existing branch-site models involving an additional ω parameter along the foreground branch, to account for the effects of both greater positive selection and greater purifying selection at different codon sites along a particular branch. The higher rates of evolution and congruent phylogenetic signal of both LEGCYC paralogs show promise for the use of these genes as markers for phylogeny reconstruction at low taxonomic levels in Genisteae.

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