Relaxed selection is a precursor to the evolution of phenotypic plasticity

Hunt, Brendan G.; Ometto, Lino; Wurm, Yannick; Shoemaker, DeWayne; Yi, Soojin V.; Keller, Laurent; Goodisman, Michael A. D.

doi:10.1073/pnas.1104825108

Cited by 147 publications

(191 citation statements)

References 69 publications

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“…Using these alignments and phylogenetic trees as inputs, the rates of selection could be determined using maximum‐likelihood models in the program CODEML in PAML (v4.8) (Yang, 2007) using the protocol of (Fang et al., 2009) and codon frequency F3X4. To accurately determine significance, Bonferroni correction was computed to account for the repeated testing of multiple branches (Fletcher & Yang, 2010; Hunt et al., 2011) where Fad had n = 2 branches and Elovl had n = 4 branches and the adjusted p‐ value = .05/ n . To detect pervasive purifying and diversifying selection, Fast UnconstrainedBayesian AppRoximation (FUBAR) (Murrell et al., 2013) was used from the HyPhy package (Pond, Frost, & Muse, 2005).…”

Section: Methodsmentioning

confidence: 99%

Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria

Surm

Toledo

Prentis

et al. 2018

Ecology and Evolution

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The biosynthesis of long‐chain polyunsaturated fatty acids (LC‐PUFAs, ≥ C20) is reliant on the action of desaturase and elongase enzymes, which are encoded by the fatty acyl desaturase (Fad) and elongation of very long‐chain fatty acid (Elovl) gene families, respectively. In Metazoa, research investigating the distribution and evolution of these gene families has been restricted largely to Bilateria. Here, we provide insights into the phylogenetic and molecular evolutionary histories of the Fad and Elovl gene families in Cnidaria, the sister phylum to Bilateria. Four model cnidarian genomes and six actiniarian transcriptomes were interrogated. Analysis of the fatty acid composition of a candidate cnidarian species, Actinia tenebrosa, was performed to determine the baseline profile of this species. Phylogenetic analysis revealed lineage‐specific gene duplication in actiniarians for both the Fad and Elovl gene families. Two distinct cnidarian Fad clades clustered with functionally characterized Δ5 and Δ6 proteins from fungal and plant species, respectively. Alternatively, only a single cnidarian Elovl clade clustered with functionally characterized Elovl proteins (Elovl4), while two additional clades were identified, one actiniarian‐specific (Novel ElovlA) and the another cnidarian‐specific (Novel ElovlB). In actiniarians, selection analyses revealed pervasive purifying selection acting on both gene families. However, codons in the Elovl gene family show patterns of nucleotide variation consistent with the action of episodic diversifying selection following gene duplication events. Significantly, these codons may encode amino acid residues that are functionally important for Elovl proteins to target and elongate different precursor fatty acids. In A. tenebrosa, the fatty acid analysis revealed an absence of LC‐PUFAs > C20 molecules and implies that the Elovl enzymes are not actively contributing to the elongation of these LC‐PUFAs. Overall, this study has revealed that actiniarians possess Fad and Elovl genes required for the biosynthesis of some LC‐PUFAs, and that these genes appear to be distinct from bilaterians.

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Section: Methodsmentioning

confidence: 99%

Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria

Surm

Toledo

Prentis

et al. 2018

Ecology and Evolution

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“…The differentiation in protein expression detected may be a result of genetic drift following a relaxation of evolutionary constraints (Khan et al 2013), selection following the colonization of a novel environment (Fraser et al 2011), founder effects (Kolbe et al 2012), and/or phenotypic plasticity (Hunt et al 2011). We did not specifically test for plasticity in this study because venom expression differences have been shown repeatedly to be under genetic control and not environmentally induced (Daltry et al 1996;Gibbs et al 2011;Holding et al 2015;Margres et al 2015b), and the feeding ecology of venomous snakes makes adaptive plasticity unlikely.…”

Section: Expression Differentiation and Variation Are Constrained To mentioning

confidence: 99%

Expression Differentiation Is Constrained to Low-Expression Proteins over Ecological Timescales

Margres¹,

Wray²,

Seavy³

et al. 2015

Genetics

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Protein expression level is one of the strongest predictors of protein sequence evolutionary rate, with high-expression protein sequences evolving at slower rates than low-expression protein sequences largely because of constraints on protein folding and function. Expression evolutionary rates also have been shown to be negatively correlated with expression level across human and mouse orthologs over relatively long divergence times (i.e., 100 million years). Long-term evolutionary patterns, however, often cannot be extrapolated to microevolutionary processes (and vice versa), and whether this relationship holds for traits evolving under directional selection within a single species over ecological timescales (i.e., ,5000 years) is unknown and not necessarily expected. Expression is a metabolically costly process, and the expression level of a particular protein is predicted to be a tradeoff between the benefit of its function and the costs of its expression. Selection should drive the expression level of all proteins close to values that maximize fitness, particularly for high-expression proteins because of the increased energetic cost of production. Therefore, stabilizing selection may reduce the amount of standing expression variation for high-expression proteins, and in combination with physiological constraints that may place an upper bound on the range of beneficial expression variation, these constraints could severely limit the availability of beneficial expression variants. To determine whether rapid-expression evolution was restricted to low-expression proteins owing to these constraints on highly expressed proteins over ecological timescales, we compared venom protein expression levels across mainland and island populations for three species of pit vipers. We detected significant differentiation in protein expression levels in two of the three species and found that rapid-expression differentiation was restricted to low-expression proteins. Our results suggest that various constraints on high-expression proteins reduce the availability of beneficial expression variants relative to lowexpression proteins, enabling low-expression proteins to evolve and potentially lead to more rapid adaptation.KEYWORDS protein expression; selective constraints; evolutionary rates; adaptation T HE expression level of a protein is one of the strongest predictors of protein sequence evolutionary rate; sequences of highly expressed proteins evolve more slowly than low-expression proteins (Duret and Mouchiroud 1999;Pal et al. 2001;Gout et al. 2010;Yang et al. 2012;Nabholz et al. 2013;Park et al. 2013). This relationship may be a function of specific selective constraints on sequences to avoid protein misfolding (Drummond et al. 2005;Geiler-Samerotte et al. 2011), protein misinteractions (Yang et al. 2012, a decrease in protein function (Cherry 2010;Gout et al. 2010), and/or messenger RNA (mRNA) misfolding (Park et al. 2013). Analyses of microarray data have shown that expression evolutionary rate is also negatively...

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“…Alternatively, size diversity could primarily evolve through relaxed selective pressures on worker size provided by social life. Relaxing selective pressures is known to decrease developmental canalization (the developmental processes that keep the phenotype constant in spite of genetic or environmental variation, see Debat and David 2001) and could hence increase worker size diversity (Hunt et al 2011). In ants, worker size diversity could result from the active process of workers providing different environmental conditions to larvae and/or from developmental response of larvae to external environmental factors as observed in the ant Messor pergandei where larvae develop into workers of different sizes depending on the season (Rissing 1987).…”

Section: Introductionmentioning

confidence: 99%

“…They are generally the product of phenotypic plasticity (e.g. Sumner et al 2006;Hunt et al 2011;Linksvayer at al. 2011; but see Schwander et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Decreasing worker size diversity does not affect colony performance during laboratory challenges in the ant Temnothorax nylanderi

Colin

Doums

Péronnet

et al. 2017

Behav Ecol Sociobiol

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Authors' contributions TC collected colonies, reared them, performed the experiments and statistical analyses, and wrote the manuscript. CD designed the study, contributed to statistical analysis and wrote the manuscript. RP collected colonies, and assisted in rearing and experiments. MM designed the study, wrote the manuscript, and supervised the project. All authors read and approved the final manuscript. Within-colony phenotypic diversity can play an essential role in some eusocial insect taxa by increasing the performance of division of labor, thereby increasing colony fitness. Empirical studies of the effect of phenotypic diversity on colony fitness mostly focused on species with discrete castes (workers, soldiers) or with continuously and highly morphologically variable workers, which is not the most common case. Indeed, most species exhibit continuous but limited worker morphological variation. It is still unclear whether this variation impacts colony fitness. To test this, we reduced the worker size diversity in 25 colonies of the ant Temnothorax nylanderi and compared their performances to 25 control colonies. We reared these colonies in the laboratory and measured the effect of treatment (reduced diversity or control) and colony size (number of workers) on colony performance at six challenges, as well as on worker mortality and brood production. The reduction of worker size diversity did not affect colony performance nor mortality and brood production. As expected, colony performance and brood production increased with colony size. These results suggest that worker size diversity may not be under positive selection in this species, but rather the product of a lack of developmental canalization. We propose that social life could decrease the selective pressures maintaining developmental canalization, subsequently leading to higher size diversity without necessarily increasing colony performance. 4 Significance statementIn social insects, nestmate size diversity is commonly thought to improve division of labour and colony performance. This has been clearly demonstrated in species with high size diversity, either discrete or continuous, but this is unclear in most of the social insects that exhibit low size diversity. We experimentally decreased worker size diversity in the ant Temnothorax nylanderi, a species with low worker size diversity. Reducing worker size diversity had no effect on colony performance, worker mortality or brood production. Our findings support the hypothesis that low size diversity is merely the product of developmental noise and is not necessarily adaptive. We propose that social life could relax the selective pressures maintaining developmental and social canalizations, subsequently leading to size diversity.5

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Relaxed selection is a precursor to the evolution of phenotypic plasticity

Cited by 147 publications

References 69 publications

Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria

Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria

Expression Differentiation Is Constrained to Low-Expression Proteins over Ecological Timescales

Decreasing worker size diversity does not affect colony performance during laboratory challenges in the ant Temnothorax nylanderi

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