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Curr Biol
2010 Jan 26;202:125-30. doi: 10.1016/j.cub.2009.11.015.
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Identical skin toxins by convergent molecular adaptation in frogs.
Roelants K
,
Fry BG
,
Norman JA
,
Clynen E
,
Schoofs L
,
Bossuyt F
.
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The Tree of Life is rife with adaptive convergences at all scales and biological levels of complexity. However, natural selection is not likely to result in the independent evolution of identical gene products. Here we report such a striking example of evolutionary convergence in the toxic skin secretions of two distantly related frog lineages. Caeruleins are important decapeptides in pharmacological and clinical research [1] and are commonly believed to represent a single evolutionary class of peptides [2-4]. Instead, our phylogenetic analyses combining transcriptome and genome data reveal that independently evolved precursor genes encode identical caeruleins in Xenopus and Litoria frogs. The former arose by duplication from the cholecystokinin (cck) gene, whereas the latter was derived from the gastrin gene. These hormone genes that are involved in many physiological processes diverged early in vertebrate evolution, after a segmental duplication during the Cambrian period. Besides implicating convergent mutations of the peptide-encoding sequence, recurrent caerulein origins entail parallel shifts of expression from the gut-brain axis to skin secretory glands. These results highlight extreme structural convergence in anciently diverged genes as an evolutionary mechanism through which recurrent adaptation is attained across large phylogenetic distances.
Figure 1.
Comparative Alignments of the Newly Identified Precursors with Known Amphibian CCK, Gastrin, and Caerulein Precursors
(A) Amino acid sequence alignment of the S. tropicalis XT-6 like precursor (XT6LP) with amphibian CCK precursors and an X. laevis caerulein precursor (XLCAE3P). The sequence of XLCAE3P occupies multiple lines because duplicated exons were aligned to each other. Numbers in parentheses indicate XLCAE3LP exon ends.
(B) Gene structure comparison of the xt6lp gene with the cck and xlcae3p genes.
(C) Amino acid sequence alignment of the Litoria splendida caerulein 1 precursor (LSCAE1P) with amphibian gastrin.
The newly identified precursors are labeled in lime green. In (A) and (C), amino acid residues are highlighted as follows: dark gray, shared between caerulein precursors and others; light gray, shared between XT6LP and CCK precursors; orange, XT-6 isoform; blue, caerulein peptides. Predicted signal peptides are printed in lowercase. In (B), homologous exons and peptide regions are shown in the same color scheme. SP indicates signal peptide.
Figure 2.
Phylogeny and Comparative Genomics of the Vertebrate cck/gastrin Gene Family
Left: parallel origins of caerulein are indicated in light blue. Inferred duplication events are labeled “D.” Branch labels represent bootstrap percentages obtained by maximum parsimony (left) and maximum likelihood (right); values < 50% are indicated by a slash (/). Gray and black bootstrap percentages are calculated from data sets 1 and 2, respectively (see Results). The phylogeny is time calibrated with a Bayesian relaxed-clock model and priors for vertebrate divergence times derived from the fossil record and molecular studies (see Supplemental Experimental Procedures). Black horizontal bars in the timescale represent 95% credibility intervals for two relevant duplication events (nodes D1 and D2). Branches along which skin expression evolved are indicated in orange. Right: cck and gastrin genes of various vertebrates and xt6lp of S. tropicalis (filled and empty dark green symbols in the synteny maps) are flanked by homologous gene pairs (vertically aligned filled and empty symbols; see gene identity legend for color code), providing evidence for a segmental duplication (node D1) in the ancestor of jawed vertebrates. Depicted genes were included in data set 2. The following abbreviations are used: Np, Neoproterozoic; Cz, Cenozoic; CI, credibility interval; Mya, million years ago; Chr, chromosome; Scaff, scaffold.
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Convergent evolution: pick your poison carefully.
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