Wollenberg Valero KC et al. (2017), Transcriptomic and macroevolutionary evidence f...

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Nat Commun 2017 May 15;8:15213. doi: 10.1038/ncomms15213.

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Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases.

Wollenberg Valero KC , Garcia-Porta J , Rodríguez A , Arias M , Shah A , Randrianiaina RD , Brown JL , Glaw F , Amat F , Künzel S , Metzler D , Isokpehi RD , Vences M .

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Anuran amphibians undergo major morphological transitions during development, but the contribution of their markedly different life-history phases to macroevolution has rarely been analysed. Here we generate testable predictions for coupling versus uncoupling of phenotypic evolution of tadpole and adult life-history phases, and for the underlying expression of genes related to morphological feature formation. We test these predictions by combining evidence from gene expression in two distantly related frogs, Xenopus laevis and Mantidactylus betsileanus, with patterns of morphological evolution in the entire radiation of Madagascan mantellid frogs. Genes linked to morphological structure formation are expressed in a highly phase-specific pattern, suggesting uncoupling of phenotypic evolution across life-history phases. This gene expression pattern agrees with uncoupled rates of trait evolution among life-history phases in the mantellids, which we show to have undergone an adaptive radiation. Our results validate a prevalence of uncoupling in the evolution of tadpole and adult phenotypes of frogs.

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Species referenced: Xenopus laevis
Genes referenced: blnk c4a ctsk cyp19a1 ifitm5 il1r1 klf4 lipc lmna lpl lrp2 nmral1 nppa pafah1b1 pou2f3 ptk2b slc6a2 slco2a1 sp9 tnk2 trpv1 ttc8 tyr ugt1a6 vars2 wwp2

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	Figure 1. Predictions for coupled and uncoupled trait evolution in life-history phases. (a) ‘Phase-Pleiotropy' under coupled evolution. The same genes contribute to tadpole and adult morphological features (here: body size). Non-synonymous DNA substitutions are rare due to phase-specific selective regimes. The same genes are equally expressed across phases. Phenotypic evolutionary rates are correlated and rate changes are concentrated on the same parts of the phylogeny (t represents evolutionary time). (b) ‘Phase-Polygeny' model 1: uncoupled evolution with different genes coding for tadpole and adult phenotype. Non-synonymous DNA substitutions are common due to phase-specific selective regimes. Genes are unequally expressed across phases. Parallel genetic changes are rare, only if favored by selection across phases, and facilitated by linkage. Phenotypic evolutionary rates are not correlated and rate changes are unequally distributed on the phylogeny. (c) ‘Phase-Polygeny' model 2: uncoupled evolution with regulatory (gene expression) or epistatic changes among tadpole and adult phenotype. The same genes contribute to tadpole and adult phenotype, but are regulated/expressed differently (mRNA—bars, epistatic gene products—tear drops, crosses, grey circles). Independent changes in expression/regulation are common due to phase-specific selective regimes. Transcripts are unequally expressed across phases. Parallel changes in expression/regulation are rare, occurring only if favoured by selection across phases and facilitated by functional interactions between regulators. Phenotypic evolutionary rates are not correlated and rate changes are unequally distributed on the phylogeny.
	Figure 2. Life-history specific gene expression and contribution to phenotype in frogs. (a,b) Venn diagram showing summary statistics of genes differentially expressed between life-history phases tadpole and adult, and combinations of these in (a) Xenopus laevis (from Xenbase) and (b) Mantidactylus betsileanus (from two newly sequenced transcriptomes). Numbers in Venn diagrams: top row, number of annotated genes expressed per phase; middle row, number of genes associated with morphological feature formation expressed per phase; bottom row, percentage of morphological-feature-formation-associated genes. (c) Morphology-associated gene expression in adult and tadpole M. betsileanus shown as scatterplot of log tadpole FPKM (fragments per kilobase of exon per million reads mapped) versus log adult FPKM. Symbols denote different categories of morphology-associated gene ontology terms; if one gene has more than one term the symbols are partly overlapping. Symbol size represents combined adult and tadpole FPKM value, as shown in the stacked FPKM scale (right). Red labelled symbols denote significantly differentially expressed transcripts (protein symbols). (d) STRING subnetwork (confidence view) of functional interactions between some genes expressed in adult life phase in Xenopus (blue gene symbols) and M. betsileanus (red gene symbols). Expressed genes of both species are linked within the same functional network with ‘osteoclast differentiation' as the significantly overexpressed function. Line thickness represents strength of confidence for interactions.
	Figure 3. Phenotypic optima and uncoupling of character evolution in mantellid frogs. (a) Phylogeny showing high (red) and low (blue) relative rates of phenotypic evolution in mantellids. Black branches show no rate acceleration or deceleration. Triangles mark shifts between selective optima (black, shared in adult and tadpole phenotypes; grey, unique to either of the two phases). A, Aglyptodactylus; Bl, Blommersia; Ge, Gephyromantis; Gu, Guibemantis; Mt, Mantella; Sp, Spinomantis. The focal species Mantidactylus betsileanus is marked with an asterisk. (b) Rates of phenotypic evolution through time, showing uncoupled rates at ca. 24 and 7.5 Myr ago (indicated by a star and highlighted by grey bars). The continuous line represents adults, the hatched line tadpoles. (c) Plot of the number of shifts between selective optima through time, showing two peaks at ca. 25 and 12.5 Myr ago. The second adaptive peak is characterized by uncoupling of shifts between adults and tadpoles (star). (d) Variation of the diversification rate (in orange) and the predicted increase of species richness (in blue) according to the best-supported diversification model found in our study (model 3). This model of diversification assumes an exponential variation of speciation rate with no extinction. (e) Disparity through time (DTT) plots visualizing the dynamics of phenotypic diversification in adults and tadpoles of the family Mantellidae, for the first MDS variable. See Supplementary Fig. 5 for full plots including comparisons with simulated curves. Inset photos show representative mantellids.

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Ashburner, Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. 2000, Pubmed