Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.     

Simulating the evolution of a clonal trait in plants with sexual and vegetative reproduction

Aims Phenotypic optimality models neglect genetics. However, especially when heterozygous genotypes are fittest, evolving allele, genotype and phenotype frequencies may not correspond to predicted optima. This was not previously addressed for organisms with complex life histories.Methods Therefore, we modelled the evolution of a fitness-relevant trait of clonal plants, stolon internode length. We explored the likely case of an asymmetric unimodal fitness profile with three model types. In constant selection models (CSMs), which are gametic, but not spatially explicit, evolving allele frequencies in the one-locus and five-loci cases did not correspond to optimum stolon internode length predicted by the spatially explicit, but not gametic, phenotypic model. This deviation was due to the asymmetry of the fitness profile. Gametic, spatially explicit individual-based (SEIB) modeling allowed us relaxing the CSM assumptions of constant selection with exclusively sexual reproduction.Important findings For entirely vegetative or sexual reproduction, predictions of the gametic SEIB model were close to the ones of spatially explicit non-gametic phenotypic models, but for mixed modes of reproduction they approximated those of gametic, not spatially explicit CSMs. Thus, in contrast to gametic SEIB models, phenotypic models and, especially for few loci, also CSMs can be very misleading. We conclude that the evolution of traits governed by few quantitative trait loci appears hardly predictable by simple models, that genetic algorithms aiming at technical optimization may actually miss the optimum and that selection may lead to loci with smaller effects in derived compared with ancestral lines.     

Correlated evolution of senescence and ephemeral substrate use in the Sordariomycetes

Evolutionary theory predicts that senescence--a decline in reproduction and survival with increasing age--can evolve as a trade-off between investment in reproduction on one side and in somatic maintenance and repair on the other. The ecology of a species is crucial because it provides the external causes of death that determine the statistical limit to a species' lifespan. Filamentous fungi are generally believed to be nonsenescent, and there are indeed spectacular examples of very old fungal individuals in nature. However, some fungi utilize ephemeral resources, and therefore, senescence is expected to have evolved, like in the coprophilic Podospora anserina, the only well-studied filamentous fungus with intrinsic senescence. Here, we hypothesize that rapid senescence is more common in fungi than generally believed and that the phylogenetic distribution of senescence correlates with ecology. We collected lifespan data for a set of Sordariomycetes and constructed phylogenies based on several nuclear sequences. Several of the strains were from the CBS culture collection, originally isolated from various substrates, some of which ephemeral. In addition, we isolated new strains from short-lived substrates. Senescence was observed throughout the phylogeny. Correlation tests support the hypothesis that in the Sordariomycetes, senescence is a trait that has arisen in response to ephemeral substrates, and that it has evolved repeatedly and independently along the phylogeny.     

Simulating DNA coding sequence evolution with EvolveAGene 3

Phylogenetic reconstruction based upon multiple alignments ofmolecular sequences is important to most branches of modernbiology and is central to molecular evolution. Understandingthe historical relationships among macromolecules depends uponcomputer programs that implement a variety of analytical methods.Because it is impossible to know those historical relationshipswith certainty, assessment of the accuracy of methods and theprograms that implement them requires the use of programs thatrealistically simulate the evolution of DNA sequences. EvolveAGene3 is a realistic coding sequence simulation program that separatesmutation from selection and allows the user to set selectionconditions, including variable regions of selection intensitywithin the sequence and variation in intensity of selectionover branches. Variation includes base substitutions, insertions,and deletions. To the best of my knowledge, it is the only programavailable that simulates the evolution of intact coding sequences.Output includes the true tree and true alignments of the resultingcoding sequence and corresponding protein sequences. A log filereports the frequencies of each kind of base substitution, theratio of transition to transversion substitutions, the ratioof indel to base substitution mutations, and the numbers ofsilent and amino acid replacement mutations. The realism ofthe data sets has been assessed by comparing the d_N/d_S ratio,the ratio of transition to transversion substitutions, and theratio of indel to base substitution mutations of the simulateddata sets with those parameters of real data sets from the "goldstandard" BaliBase collection of structural alignments. Resultsshow that the data sets produced by EvolveAGene 3 are very similarto real data sets, and EvolveAGene 3 is therefore a realisticsimulation program that can be used to evaluate a variety ofprograms and methods in molecular evolution.     

Ancestrality and evolution of trait syndromes in finches (Fringillidae)

Species traits have been hypothesized by one of us (Ponge, 2013) to evolve in a correlated manner as species colonize stable, undisturbed habitats, shifting from “ancestral” to “derived” strategies. We predicted that generalism, r‐selection, sexual monomorphism, and migration/gregariousness are the ancestral states (collectively called strategy A) and evolved correlatively toward specialism, K‐selection, sexual dimorphism, and residence/territoriality as habitat stabilized (collectively called B strategy). We analyzed the correlated evolution of four syndromes, summarizing the covariation between 53 traits, respectively, involved in ecological specialization, r‐K gradient, sexual selection, and dispersal/social behaviors in 81 species representative of Fringillidae, a bird family with available natural history information and that shows variability for all these traits. The ancestrality of strategy A was supported for three of the four syndromes, the ancestrality of generalism having a weaker support, except for the core group Carduelinae (69 species). It appeared that two different B‐strategies evolved from the ancestral state A, both associated with highly predictable environments: one in poorly seasonal environments, called B1, with species living permanently in lowland tropics, with “slow pace of life” and weak sexual dimorphism, and one in highly seasonal environments, called B2, with species breeding out‐of‐the‐tropics, migratory, with a “fast pace of life” and high sexual dimorphism.     

Correlated evolution of multivariate traits: detecting co-divergence across multiple dimensions

Tests of correlated evolution typically treat phenotypic characters as univariate variables, even though different trait attributes may contribute to their association with other traits. In this study, patterns of character covariation among species are analysed in a multivariate framework to test for both correlated rates and directions of evolutionary change in traits forming the genitalic complex of male grasshoppers. Although the covariation structure differs among traits, and among the constituent species of two grasshopper clades, significant co-divergence was detected among the most closely interacting genitalic traits (i.e. intromittent characters) in both clades. Co-divergence across shape space is not accompanied by similar rates of evolution among species, although the intromittent characters tend to show accelerated evolution (relative to nonintromittent characters). Differences in the evolutionary trajectories among traits may relate to their varied roles during mating. The study emphasizes the importance of a multivariate framework for detecting macroevolutionary patterns of correlated change.     

The phylogeny of the Pentaschistis clade (Danthonioideae, Poaceae) based on chloroplast DNA, and the evolution and loss of complex characters

We construct a species-level phylogeny for the Pentaschistis clade based on chloroplast DNA, from the following regions: trnL-F, trnT-L, atpB-rbcL, rpL16, and trnD-psbA. The clade comprises 82 species in three genera, Pentaschistis, Pentameris, and Prionanthium. We demonstrate that Prionanthium is nested in Pentaschistis and that this clade is sister to a clade of Pentameris plus Pentaschistis tysonii. Forty-three of the species in the Pentaschistis clade have multicellular glands and we use ancestral character state reconstruction to show that they have been gained twice or possibly once, and lost several times. We suggest that the maintenance, absence, loss, and gain of glands are correlated with leaf anatomy type, and additionally that there is a difference in the degree of diversification of lineages that have these different character combinations. We propose that both glands and sclerophyllous leaves act as defense systems against herbivory, and build a cost/benefit model in which multicellular glands or sclerophyllous leaves are lost when the alternative defense system evolves. We also investigate the association between leaf anatomy type and soil nutrient type on which species grow. There is little phylogenetic constraint in soil nutrient type on members of the Pentaschistis clade, with numerous transitions between oligotrophic and eutrophic soils. However, only orthophyllous-leaved species diversify on eutrophic soils. We suggest that the presence of these glands enables the persistence of orthophyllous lineages and therefore diversification of the Pentaschistis clade on eutrophic as well as oligotrophic soils.     

THE USEFULNESS OF BEHAVIOR FOR PHYLOGENY ESTIMATION: LEVELS OF HOMOPLASY IN BEHAVIORAL AND MORPHOLOGICAL CHARACTERS

It is widely believed that behavior is more evolutionarily labile and/or more difficult to characterize than morphology, and thus that behavioral characters are not as useful as morphological characters for estimating phylogenetic relationships. To examine the relative utility of behavior and morphology for estimating phylogeny, we compared levels of homoplasy for morphological and behavioral characters that have been used in systematic studies. In an analysis of 22 data sets that contained both morphological and behavioral characters we found no significant difference between mean consistency indices (CIs, which measure homoplasy) within data sets for the two types of characters. In a second analysis we compared overall CIs for 8 data sets comprised entirely of behavioral characters with overall CIs for 32 morphological data sets and found no significant difference between the two types of data sets. For both analyses, 95% confidence limits on the difference between the two types of characters indicate that, even if given the benefit of the doubt, morphological characters could not have substantially higher mean CIs than behavioral characters. These results do not support the idea that behavioral characters are less useful than morphological characters for the estimation of phylogeny.     

Divergence and evolution of assortative mating in a polygenic trait model of speciation with gene flow

Assortative mating is an important driver of speciation in populations with gene flow and is predicted to evolve under certain conditions in few‐locus models. However, the evolution of assortment is less understood for mating based on quantitative traits, which are often characterized by high genetic variability and extensive linkage disequilibrium between trait loci. We explore this scenario for a two‐deme model with migration, by considering a single polygenic trait subject to divergent viability selection across demes, as well as assortative mating and sexual selection within demes, and investigate how trait divergence is shaped by various evolutionary forces. Our analysis reveals the existence of sharp thresholds of assortment strength, at which divergence increases dramatically. We also study the evolution of assortment via invasion of modifiers of mate discrimination and show that the ES assortment strength has an intermediate value under a range of migration‐selection parameters, even in diverged populations, due to subtle effects which depend sensitively on the extent of phenotypic variation within these populations. The evolutionary dynamics of the polygenic trait is studied using the hypergeometric and infinitesimal models. We further investigate the sensitivity of our results to the assumptions of the hypergeometric model, using individual‐based simulations.     

Uncorrelated evolution between vocal and plumage coloration traits in the trogons: a comparative study

The costs of bird song incurred in a diversity of ways may result in trade‐offs in the production and maintenance of elaborate plumage ornaments. In this paper, we examine evolutionary trade‐offs between acoustic and visual signalling in trogon birds (Trogonidae). Using multiple regressions with phylogenetically independent contrasts, we found that interspecific variation in male plumage coloration was not significantly predicted by song traits (reduced by PCA) or altitude. Although plumage coloration is expected to decrease with increases in song elaboration, both groups of variables were not related. Given that song and plumage coloration traits are likely targets of sexual selection, we also examined their relationships with sexual plumage dimorphism. We found that male carotenoid‐derived coloration was positively related to sexual plumage dimorphism, suggesting that sexual selection on male carotenoid‐derived coloration may be stronger than on melanin‐ or structurally based coloration, or than on acoustic traits. Comparative studies on other bird families accounting for the effects of phylogeny as well as environmental covariates are required to test the generality of our findings in trogons.     

Cultural evolution: implications for understanding the human language faculty and its evolution

Human language is unique among the communication systems of the natural world: it is socially learned and, as a consequence of its recursively compositional structure, offers open-ended communicative potential. The structure of this communication system can be explained as a consequence of the evolution of the human biological capacity for language or the cultural evolution of language itself. We argue, supported by a formal model, that an explanatory account that involves some role for cultural evolution has profound implications for our understanding of the biological evolution of the language faculty: under a number of reasonable scenarios, cultural evolution can shield the language faculty from selection, such that strongly constraining language-specific learning biases are unlikely to evolve. We therefore argue that language is best seen as a consequence of cultural evolution in populations with a weak and/or domain-general language faculty.     

Theoretical foundation of the balanced minimum evolution method of phylogenetic inference and its relationship to weighted least-squares tree fitting

Due to its speed, the distance approach remains the best hope for building phylogenies on very large sets of taxa. Recently (R. Desper and O. Gascuel, J. Comp. Biol. 9:687-705, 2002), we introduced a new "balanced" minimum evolution (BME) principle, based on a branch length estimation scheme of Y. Pauplin (J. Mol. Evol. 51:41-47, 2000). Initial simulations suggested that FASTME, our program implementing the BME principle, was more accurate than or equivalent to all other distance methods we tested, with running time significantly faster than Neighbor-Joining (NJ). This article further explores the properties of the BME principle, and it explains and illustrates its impressive topological accuracy. We prove that the BME principle is a special case of the weighted least-squares approach, with biologically meaningful variances of the distance estimates. We show that the BME principle is statistically consistent. We demonstrate that FASTME only produces trees with positive branch lengths, a feature that separates this approach from NJ (and related methods) that may produce trees with branches with biologically meaningless negative lengths. Finally, we consider a large simulated data set, with 5,000 100-taxon trees generated by the Aldous beta-splitting distribution encompassing a range of distributions from Yule-Harding to uniform, and using a covarion-like model of sequence evolution. FASTME produces trees faster than NJ, and much faster than WEIGHBOR and the weighted least-squares implementation of PAUP*. Moreover, FASTME trees are consistently more accurate at all settings, ranging from Yule-Harding to uniform distributions, and all ranges of maximum pairwise divergence and departure from molecular clock. Interestingly, the covarion parameter has little effect on the tree quality for any of the algorithms. FASTME is freely available on the web.     

Testing for different rates of continuous trait evolution using likelihood

Rates of phenotypic evolution have changed throughout the history of life, producing variation in levels of morphological, functional, and ecological diversity among groups. Testing for the presence of these rate shifts is a key component of evaluating hypotheses about what causes them. In this paper, general predictions regarding changes in phenotypic diversity as a function of evolutionary history and rates are developed, and tests are derived to evaluate rate changes. Simulations show that these tests are more powerful than existing tests using standardized contrasts. The new approaches are distributed in an application called Brownie and in r8s.     

Infectious disease,behavioural flexibility and the evolution of culture in primates

Culturally transmitted traits are observed in a wide array of animal species, yet we understand little about the costs of the behavioural patterns that underlie culture, such as innovation and social learning. We propose that infectious diseases are a significant cost associated with cultural transmission. We investigated two hypotheses that may explain such a connection: that social learning and exploratory behaviours (specifically, innovation and extractive foraging) either compensate for existing infection or increase exposure to infectious agents. We used Bayesian comparative methods, controlling for sampling effort, body mass, group size, geographical range size, terrestriality, latitude and phylogenetic uncertainty. Across 127 primate species, we found a positive association between pathogen richness and rates of innovation, extractive foraging and social learning. This relationship was driven by two independent phenomena: socially contagious diseases were positively associated with rates of social learning, and environmentally transmitted diseases were positively associated with rates of exploration. Because higher pathogen burdens can contribute to morbidity and mortality, we propose that parasitism is a significant cost associated with the behavioural patterns that underpin culture, and that increased pathogen exposure is likely to have played an important role in the evolution of culture in both non-human primates and humans.     

Quantifying hummingbird preference for floral trait combinations: The role of selection on trait interactions in the evolution of pollination syndromes

Darwin recognized the flower's importance for the study of adaptation and emphasized that the flower's functionality reflects the coordinated action of multiple traits. Here we use a multitrait manipulative approach to quantify the potential role of selection acting on floral trait combinations underlying the divergence and maintenance of three related North American species of Silene (Caryophyllaceae). We artificially generated 48 plant phenotypes corresponding to all combinations of key attractive traits differing among the three Silene species (color, height, inflorescence architecture, flower orientation, and corolla‐tube width). We quantified main and interaction effects of trait manipulation on hummingbird visitation preference using experimental arrays. The main effects of floral display height and floral orientation strongly influenced hummingbird visitation, with hummingbirds preferring flowers held high above the ground and vertically to the sky. Hummingbirds also prefer traits in a nonadditive manner as multiple two‐way and higher order interaction effects were important predictors of hummingbird visitation. Contemporary trait combinations found in hummingbird pollinated S. virginica are mostly preferred. Our study demonstrates the likelihood of pollination syndromes evolving due to selection on trait combinations and highlights the importance of trait interactions in understanding the evolution of complex adaptations.     

Multidimensional vector space representation for convergent evolution and molecular phylogeny

With growing amounts of genome data and constant improvement of models of molecular evolution, phylogenetic reconstruction became more reliable. However, our knowledge of the real process of molecular evolution is still limited. When enough large-sized data sets are analyzed, any subtle biases in statistical models can support incorrect topologies significantly because of the high signal-to-noise ratio. We propose a procedure to locate sequences in a multidimensional vector space (MVS), in which the geometry of the space is uniquely determined in such a way that the vectors of sequence evolution are orthogonal among different branches. In this paper, the MVS approach is developed to detect and remove biases in models of molecular evolution caused by unrecognized convergent evolution among lineages or unexpected patterns of substitutions. Biases in the estimated pairwise distances are identified as deviations (outliers) of sequence spatial vectors from the expected orthogonality. Modifications to the estimated distances are made by minimizing an index to quantify the deviations. In this way, it becomes possible to reconstruct the phylogenetic tree, taking account of possible biases in the model of molecular evolution. The efficacy of the modification procedure was verified by simulating evolution on various topologies with rate heterogeneity and convergent change. The phylogeny of placental mammals in previous analyses of large data sets has varied according to the genes being analyzed. Systematic deviations caused by convergent evolution were detected by our procedure in all representative data sets and were found to strongly affect the tree structure. However, the bias correction yielded a consistent topology among data sets. The existence of strong biases was validated by examining the sites of convergent evolution between the hedgehog and other species in mitochondrial data set. This convergent evolution explains why it has been difficult to determine the phylogenetic placement of the hedgehog in previous studies.