Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.     

Diversity and phylogeny of Baltic Sea picocyanobacteria inferred from their ITS and phycobiliprotein operons

Picocyanobacteria of the genus Synechococcus span a range of different colours, from red strains rich in phycoerythrin (PE) to green strains rich in phycocyanin (PC). Here, we show that coexistence of red and green picocyanobacteria in the Baltic Sea is widespread. The diversity and phylogeny of red and green picocyanobacteria was analysed using three different genes: 16S rRNA-ITS, the cpeBA operon of the red PE pigment and the cpcBA operon of the green PC pigment. Sequencing of 209 clones showed that Baltic Sea picocyanobacteria exhibit high levels of microdiversity. The partial nucleotide sequences of the cpcBA and cpeBA operons from the clone libraries of the Baltic Sea revealed two distinct phylogenetic clades: one clade containing mainly sequences from cultured PC-rich picocyanobacteria, while the other contains only sequences from cultivated PE-rich strains. A third clade of phycourobilin (PUB) containing strains of PE-rich Synechococcus spp. did not contain sequences from the Baltic Sea clone libraries. These findings differ from previously published phylogenies based on 16S rRNA gene analysis. Our data suggest that, in terms of their pigmentation, Synechococcus spp. represent three different lineages occupying different ecological niches in the underwater light spectrum. Strains from different lineages can coexist in light environments that overlap with their light absorption spectra.     

Stabilizing selection and adaptive evolution in a combination of two traits in an arctic ungulate

Stabilizing selection is thought to be common in wild populations and act as one of the main evolutionary mechanisms, which constrain phenotypic variation. When multiple traits interact to create a combined phenotype, correlational selection may be an important process driving adaptive evolution. Here, we report on phenotypic selection and evolutionary changes in two natal traits in a semidomestic population of reindeer (Rangifer tarandus) in northern Finland. The population has been closely monitored since 1969, and detailed data have been collected on individuals since they were born. Over the length of the study period (1969–2015), we found directional and stabilizing selection toward a combination of earlier birth date and heavier birth mass with an intermediate optimum along the major axis of the selection surface. In addition, we demonstrate significant changes in mean traits toward earlier birth date and heavier birth mass, with corresponding genetic changes in breeding values during the study period. Our results demonstrate evolutionary changes in a combination of two traits, which agree closely with estimated patterns of phenotypic selection. Knowledge of the selective surface for combinations of genetically correlated traits are vital to predict how population mean phenotypes and fitness are affected when environments change.     

CHAOS AND UNPREDICTABILITY IN EVOLUTION

The possibility of complicated dynamic behavior driven by nonlinear feedbacks in dynamical systems has revolutionized science in the latter part of the last century. Yet despite examples of complicated frequency dynamics, the possibility of long‐term evolutionary chaos is rarely considered. The concept of “survival of the fittest” is central to much evolutionary thinking and embodies a perspective of evolution as a directional optimization process exhibiting simple, predictable dynamics. This perspective is adequate for simple scenarios, when frequency‐independent selection acts on scalar phenotypes. However, in most organisms many phenotypic properties combine in complicated ways to determine ecological interactions, and hence frequency‐dependent selection. Therefore, it is natural to consider models for evolutionary dynamics generated by frequency‐dependent selection acting simultaneously on many different phenotypes. Here we show that complicated, chaotic dynamics of long‐term evolutionary trajectories in phenotype space is very common in a large class of such models when the dimension of phenotype space is large, and when there are selective interactions between the phenotypic components. Our results suggest that the perspective of evolution as a process with simple, predictable dynamics covers only a small fragment of long‐term evolution.     

Ecological causes of morphological evolution in the three‐spined stickleback

The central assumption of evolutionary theory is that natural selection drives the adaptation of populations to local environmental conditions, resulting in the evolution of adaptive phenotypes. The three‐spined stickleback (Gasterosteus aculeatus) displays remarkable phenotypic variation, offering an unusually tractable model for understanding the ecological mechanisms underpinning adaptive evolutionary change. Using populations on North Uist, Scotland we investigated the role of predation pressure and calcium limitation on the adaptive evolution of stickleback morphology and behavior. Dissolved calcium was a significant predictor of plate and spine morph, while predator abundance was not. Stickleback latency to emerge from a refuge varied with morph, with populations with highly reduced plates and spines and high predation risk less bold. Our findings support strong directional selection in three‐spined stickleback evolution, driven by multiple selective agents.     

Developmental Dynamics and G-Matrices: Can Morphometric Spaces be Used to Model Phenotypic Evolution?

Modern morphometrics, especially geometric morphometrics, is a powerful tool for modeling the evolution and development of the phenotype. Complicated morphological transformations can be simulated by using standard evolutionary genetic equations for processes such as selection and drift in the same morphospaces that are used for empirical morphometric studies. Such applications appear to be consistent with the theory of quantitative evolution of the phenotype. Nevertheless, concerns exist whether simulations of phenotypic changes directly in morphospaces is realistic because trajectories traced in such spaces describe continuous gradations in the phenotype and because the gain and loss of structures is often impossible because morphospaces are necessarily constructed from variables shared in common by all the phenotypes being considered. Competing models of phenotypic change emphasize morphological discontinuity and novelty. Recently developed models of phenotypic evolution that introduce a “phenotypic landscape” between evolutionary genetic constructs like the adaptive landscape and morphospace may correct this shortcoming.     

Genome reduction by deletion of paralogs in the marine cyanobacterium Prochlorococcus

Several isolates of the marine cyanobacterial genus Prochlorococcus have smaller genome sizes than those of the closely related genus Synechococcus. In order to test whether loss of protein-coding genes has contributed to genome size reduction in Prochlorococcus, we reconstructed events of gene family evolution over a strongly supported phylogeny of 12 Prochlorococcus genomes and 9 Synechococcus genomes. Significantly, more events both of loss of paralogs within gene families and of loss of entire gene families occurred in Prochlorococcus than in Synechococcus. The number of nonancestral gene families in genomes of both genera was positively correlated with the extent of genomic islands (GIs), consistent with the hypothesis that horizontal gene transfer (HGT) is associated with GIs. However, even when only isolates with comparable extents of GIs were compared, significantly more events of gene family loss and of paralog loss were seen in Prochlorococcus than in Synechococcus, implying that HGT is not the primary reason for the genome size difference between the two genera.     

Glucosylglycerate: a secondary compatible solute common to marine cyanobacteria from nitrogen-poor environments

The synthesis and accumulation of compatible solutes represent an essential part of the salt acclimation strategy of microorganisms. Glucosylglycerol is considered to be the typical compatible solute among marine cyanobacteria. However, genes that encode enzymes for the synthesis of glucosylglycerol were not detected in the genome sequences of marine picoplanktonic Prochlorococcus strains. Instead, we noticed the presence of genes that putatively encode for glucosylglycerate (GGA) synthesis among Prochlorococcus and most other closely related marine picocyanobacteria. Recombinant proteins from Prochlorococcus marinus SS120 and Synechococcus sp. PCC 7002 exhibited glucosyl-phosphoglycerate synthase (GpgS) activity, and GpgS is a key enzyme of GGA synthesis. GGA accumulation was found to be salt- as well as nitrogen-regulated in the coastal strain Synechococcus sp. PCC 7002. Moreover, GGA was also detected in all picoplanktonic Prochlorococcus and Synechococcus strains harbouring gpgS genes, especially under N-limiting conditions. These results suggest that marine picocyanobacteria acquired the capacity to synthesize the negatively charged compound GGA during their evolution. Our results establish GGA as the fifth most widespread compatible solute among cyanobacteria. Additionally, GGA appears to replace glutamate as an anion to counter monovalent cations in marine picocyanobacteria from N-poor environments.     

Genetic evolution,plasticity, and bet‐hedging as adaptive responses to temporally autocorrelated fluctuating selection: A quantitative genetic model

Adaptive responses to autocorrelated environmental fluctuations through evolution in mean reaction norm elevation and slope and an independent component of the phenotypic variance are analyzed using a quantitative genetic model. Analytic approximations expressing the mutual dependencies between all three response modes are derived and solved for the joint evolutionary outcome. Both genetic evolution in reaction norm elevation and plasticity are favored by slow temporal fluctuations, with plasticity, in the absence of microenvironmental variability, being the dominant evolutionary outcome for reasonable parameter values. For fast fluctuations, tracking of the optimal phenotype through genetic evolution and plasticity is limited. If residual fluctuations in the optimal phenotype are large and stabilizing selection is strong, selection then acts to increase the phenotypic variance (bet‐hedging adaptive). Otherwise, canalizing selection occurs. If the phenotypic variance increases with plasticity through the effect of microenvironmental variability, this shifts the joint evolutionary balance away from plasticity in favor of genetic evolution. If microenvironmental deviations experienced by each individual at the time of development and selection are correlated, however, more plasticity evolves. The adaptive significance of evolutionary fluctuations in plasticity and the phenotypic variance, transient evolution, and the validity of the analytic approximations are investigated using simulations.     

Natural selection. VI. Partitioning the information in fitness and characters by path analysis

Three steps aid in the analysis of selection. First, describe phenotypes by their component causes. Components include genes, maternal effects, symbionts and any other predictors of phenotype that are of interest. Second, describe fitness by its component causes, such as an individual's phenotype, its neighbours’ phenotypes, resource availability and so on. Third, put the predictors of phenotype and fitness into an exact equation for evolutionary change, providing a complete expression of selection and other evolutionary processes. The complete expression separates the distinct causal roles of the various hypothesized components of phenotypes and fitness. Traditionally, those components are given by the covariance, variance and regression terms of evolutionary models. I show how to interpret those statistical expressions with respect to information theory. The resulting interpretation allows one to read the fundamental equations of selection and evolution as sentences that express how various causes lead to the accumulation of information by selection and the decay of information by other evolutionary processes. The interpretation in terms of information leads to a deeper understanding of selection and heritability, and a clearer sense of how to formulate causal hypotheses about evolutionary process. Kin selection appears as a particular type of causal analysis that partitions social effects into meaningful components.     

COMPARATIVE MOLECULAR EVOLUTION OF NEWLY DISCOVERED PICOCYANOBACTERIAL STRAINS REVEALS A PHYLOGENETICALLY INFORMATIVE VARIABLE REGION OF β‐PHYCOERYTHRIN1

The genetic diversity and phylogenetic position of 10 strains of picocyanobacteria from the Arabian Sea were examined using partial sequences from three loci: 16S rDNA, RNA polymerase rpoC1, and two elements of the phycoerythrin (PE) locus, cpeA and cpeB which encode for the α and β subunit of PE. Nine of the strains showed nearly identical spectral phenotypes based on the in vivo excitation spectrum for PE fluorescence emission and appear to be strains synthesizing a phycourobilin (PUB)–lacking PE. These strains include one, Synechococcus sp. G2.1, already known to be closely related to filamentous cyanobacteria and not to the commonly studied 5.1 subcluster of marine Synechococcus. The 10th strain was a PE‐lacking strain that was of interest because it was isolated from open‐ocean conditions where picocyanobacteria with this phenotype are relatively uncommon. Phylogenetic analysis of the concatenated 16S rDNA and rpoC1 data sets showed that none of the previously described strains were members of the 5.1 subcluster of marine Synechococcus, nor were they closely related to strain G2.1. Instead, they form a well‐supported and previously undescribed clade of cyanobacteria that is sister to Cyanobium. Thus, these strains represent the first PE‐containing Cyanobium from oceanic waters, and the lineage they define includes a strain with a PE‐lacking phenotype from the same environment. Analysis of the PE sequence data showed the PE apoprotein has evolved independently in the G2.1 lineage and the Cyanobium‐like lineage represented by the study strains. It also revealed a hypervariable region of the β‐subunit not described previously; variation in this region shows a pattern among a wide range of PE‐containing organisms congruent with the phylogenetic relationships inferred from other genes. This suggests that the PUB‐lacking spectral phenotype is more likely to have evolved in distantly related phylogenetic lineages by either divergent or convergent evolution than by lateral gene transfer. Both the conserved PE gene sequences and the inferred amino acid sequences for the hypervariable region show considerable divergence among Prochlorococcus PEs, red algal PEs, PUB‐containing PEs from the marine Synechococcus 5.1 subcluster, PEs from the Cyanobium‐like strains, and PEs from other cyanobacteria (including strain G2.1). Thus, it appears that the hypervariable region of the PE gene can be used as a taxon‐specific marker.     

Picocyanobacteria containing a novel pigment gene cluster dominate the brackish water Baltic Sea

Photoautotrophic picocyanobacteria harvest light via phycobilisomes (PBS) consisting of the pigments phycocyanin (PC) and phycoerythrin (PE), encoded by genes in conserved gene clusters. The presence and arrangement of these gene clusters give picocyanobacteria characteristic light absorption properties and allow the colonization of specific ecological niches. To date, a full understanding of the evolution and distribution of the PBS gene cluster in picocyanobacteria has been hampered by the scarcity of genome sequences from fresh- and brackish water-adapted strains. To remediate this, we analysed genomes assembled from metagenomic samples collected along a natural salinity gradient, and over the course of a growth season, in the Baltic Sea. We found that while PBS gene clusters in picocyanobacteria sampled in marine habitats were highly similar to known references, brackish-adapted genotypes harboured a novel type not seen in previously sequenced genomes. Phylogenetic analyses showed that the novel gene cluster belonged to a clade of uncultivated picocyanobacteria that dominate the brackish Baltic Sea throughout the summer season, but are uncommon in other examined aquatic ecosystems. Further, our data suggest that the PE genes were lost in the ancestor of PC-containing coastal picocyanobacteria and that multiple horizontal gene transfer events have re-introduced PE genes into brackish-adapted strains, including the novel clade discovered here.     

Body-axis organization in tetrapods: a model-system to disentangle the developmental origins of convergent evolution in deep time

Convergent evolution is a central concept in evolutionary theory but the underlying mechanism has been largely debated since On the Origin of Species. Previous hypotheses predict that developmental constraints make some morphologies more likely to arise than others and natural selection discards those of the lowest fitness. However, the quantification of the role and strength of natural selection and developmental constraint in shaping convergent phenotypes on macroevolutionary timescales is challenging because the information regarding performance and development is not directly available. Accordingly, current knowledge of how embryonic development and natural selection drive phenotypic evolution in vertebrates has been extended from studies performed at short temporal scales. We propose here the organization of the tetrapod body-axis as a model system to investigate the developmental origins of convergent evolution over hundreds of millions of years. The quantification of the primary developmental mechanisms driving body-axis organization (i.e. somitogenesis, homeotic effects and differential growth) can be inferred from vertebral counts, and recent techniques of three-dimensional computational biomechanics have the necessary potential to reveal organismal performance even in fossil forms. The combination of both approaches offers a novel and robust methodological framework to test competing hypotheses on the functional and developmental drivers of phenotypic evolution and evolutionary convergence.     

Evolutionary aspects and sensitivity studies of some major gene models

Extensive biometrical and statistically oriented studies in segregation and pedigree analyses reflect current efforts to demonstrate major gene factors playing a significant role for a whole hierarchy of multifactorial diseases and related risk factors exhibiting continuous variation. The evolutionary aspects of the changes in gene frequencies of some major gene one locus models admitting a broad range of genotype-phenotype associations and different forms of selection functions are investigated. The flexibility of differences among the genotypic-phenotypic distribution can take account of variable penetrance expressivity, complex multifarious heterogeneous background effects, or partial dominance concepts. The phenotype distribution and selection function are assumed to be time invariant such that the environments with which the population interacts do not depend on either the phenotypes or the genotypes present in the population of any particular generation. Viability selection optimizing or directional acts on the phenotypic level. We consider random mating, and concentrate mostly on evaluating the nature of the equilibrium structure for the cases of “strong” and “weak” selection. For weak stabilizing selection the determinants of superior genotypic fitness in the class of phenotypic symmetric distributions reside in minimizing a combination of the phenotypic variance and the deviation of the phenotypic mean from the optimal phenotype. With equal means of central phenotype values, a canalizing selection effect signifying fitness superiority for the genotype with minimal variance is in force. For strong stabilizing selection the genotype-phenotype density at the optimal value determines the relative genotype fitness value. For directional selection the determinants of the selection realizations depend on a “standardized” deviation of the mean phenotype distributional value relative to its total variance. The effects of symmetry as against asymmetry in the genotype distributions with prescribed means and variances were investigated by numerical computations.     

SIMULATION‐BASED LIKELIHOOD APPROACH FOR EVOLUTIONARY MODELS OF PHENOTYPIC TRAITS ON PHYLOGENY

Phylogenetic comparative methods (PCMs) have been used to test evolutionary hypotheses at phenotypic levels. The evolutionary modes commonly included in PCMs are Brownian motion (genetic drift) and the Ornstein–Uhlenbeck process (stabilizing selection), whose likelihood functions are mathematically tractable. More complicated models of evolutionary modes, such as branch‐specific directional selection, have not been used because calculations of likelihood and parameter estimates in the maximum‐likelihood framework are not straightforward. To solve this problem, we introduced a population genetics framework into a PCM, and here, we present a flexible and comprehensive framework for estimating evolutionary parameters through simulation‐based likelihood computations. The method does not require analytic likelihood computations, and evolutionary models can be used as long as simulation is possible. Our approach has many advantages: it incorporates different evolutionary modes for phenotypes into phylogeny, it takes intraspecific variation into account, it evaluates full likelihood instead of using summary statistics, and it can be used to estimate ancestral traits. We present a successful application of the method to the evolution of brain size in primates. Our method can be easily implemented in more computationally effective frameworks such as approximate Bayesian computation (ABC), which will enhance the use of computationally intensive methods in the study of phenotypic evolution.     

GroEL/S Overexpression Helps to Purge Deleterious Mutations and Reduce Genetic Diversity during Adaptive Protein Evolution

Chaperones are proteins that help other proteins fold. They also affect the adaptive evolution of their client proteins by buffering the effect of deleterious mutations and increasing the genetic diversity of evolving proteins. We study how the bacterial chaperone GroE (GroEL+GroES) affects the evolution of green fluorescent protein (GFP). To this end, we subjected GFP to multiple rounds of mutation and selection for its color phenotype in four replicate Escherichia coli populations, and studied its evolutionary dynamics through high-throughput sequencing and mutant engineering. We evolved GFP both under stabilizing selection for its ancestral (green) phenotype, and to directional selection for a new (cyan) phenotype. We did so both under low and high expression of the chaperone GroE. In contrast to previous work, we observe that GroE does not just buffer but also helps purge deleterious (fluorescence reducing) mutations from evolving populations. In doing so, GroE helps reduce the genetic diversity of evolving populations. In addition, it causes phenotypic heterogeneity in mutants with the same genotype, helping to enhance their fluorescence in some cells, and reducing it in others. Our observations show that chaperones can affect adaptive evolution in more than one way.     

Selection on skewed characters and the paradox of stasis

Observed phenotypic responses to selection in the wild often differ from predictions based on measurements of selection and genetic variance. An overlooked hypothesis to explain this paradox of stasis is that a skewed phenotypic distribution affects natural selection and evolution. We show through mathematical modeling that, when a trait selected for an optimum phenotype has a skewed distribution, directional selection is detected even at evolutionary equilibrium, where it causes no change in the mean phenotype. When environmental effects are skewed, Lande and Arnold's (1983) directional gradient is in the direction opposite to the skew. In contrast, skewed breeding values can displace the mean phenotype from the optimum, causing directional selection in the direction of the skew. These effects can be partitioned out using alternative selection estimates based on average derivatives of individual relative fitness, or additive genetic covariances between relative fitness and trait (Robertson–Price identity). We assess the validity of these predictions using simulations of selection estimation under moderate sample sizes. Ecologically relevant traits may commonly have skewed distributions, as we here exemplify with avian laying date — repeatedly described as more evolutionarily stable than expected — so this skewness should be accounted for when investigating evolutionary dynamics in the wild.     

Natural selection and inheritance of breeding time and clutch size in the collared flycatcher

Many characteristics of organisms in free-living populations appear to be under directional selection, possess additive genetic variance, and yet show no evolutionary response to selection. Avian breeding time and clutch size are often-cited examples of such characters. We report analyses of inheritance of, and selection on, these traits in a long-term study of a wild population of the collared flycatcher Ficedula albicollis. We used mixed model analysis with REML estimation ("animal models") to make full use of the information in complex multigenerational pedigrees. Heritability of laying date, but not clutch size, was lower than that estimated previously using parent-offspring regressions, although for both traits there was evidence of substantial additive genetic variance (h2 = 0.19 and 0.29, respectively). Laying date and clutch size were negatively genetically correlated (rA = -0.41 +/- 0.09), implying that selection on one of the traits would cause a correlated response in the other, but there was little evidence to suggest that evolution of either trait would be constrained by correlations with other phenotypic characters. Analysis of selection on these traits in females revealed consistent strong directional fecundity selection for earlier breeding at the level of the phenotype (beta = -0.28 +/- 0.03), but little evidence for stabilising selection on breeding time. We found no evidence that clutch size was independently under selection. Analysis of fecundity selection on breeding values for laying date, estimated from an animal model, indicated that selection acts directly on additive genetic variance underlying breeding time (beta = -0.20 +/- 0.04), but not on clutch size (beta = 0.03 +/- 0.05). In contrast, selection on laying date via adult female survival fluctuated in sign between years, and was opposite in sign for selection on phenotypes (negative) and breeding values (positive). Our data thus suggest that any evolutionary response to selection on laying date is partially constrained by underlying life-history trade-offs, and illustrate the difficulties in using purely phenotypic measures and incomplete fitness estimates to assess evolution of life-history trade-offs. We discuss some of the difficulties associated with understanding the evolution of laying date and clutch size in natural populations.     

Origin of the fittest: link between emergent variation and evolutionary change as a critical question in evolutionary biology

In complex organisms, neutral evolution of genomic architecture, associated compensatory interactions in protein networks and emergent developmental processes can delineate the directions of evolutionary change, including the opportunity for natural selection. These effects are reflected in the evolution of developmental programmes that link genomic architecture with a corresponding functioning phenotype. Two recent findings call for closer examination of the rules by which these links are constructed. First is the realization that high dimensionality of genotypes and emergent properties of autonomous developmental processes (such as capacity for self-organization) result in the vast areas of fitness neutrality at both the phenotypic and genetic levels. Second is the ubiquity of context- and taxa-specific regulation of deeply conserved gene networks, such that exceptional phenotypic diversification coexists with remarkably conserved generative processes. Establishing the causal reciprocal links between ongoing neutral expansion of genomic architecture, emergent features of organisms' functionality, and often precisely adaptive phenotypic diversification therefore becomes an important goal of evolutionary biology and is the latest reincarnation of the search for a framework that links development, functioning and evolution of phenotypes. Here I examine, in the light of recent empirical advances, two evolutionary concepts that are central to this framework-natural selection and inheritance-the general rules by which they become associated with emergent developmental and homeostatic processes and the role that they play in descent with modification.