Positive correlation between diversification rates and phenotypic evolvability can mimic punctuated equilibrium on molecular phylogenies

The hypothesis of punctuated equilibrium proposes that most phenotypic evolution occurs in rapid bursts associated with speciation events. Several methods have been developed that can infer punctuated equilibrium from molecular phylogenies in the absence of paleontological data. These methods essentially test whether the variance in phenotypes among extant species is better explained by evolutionary time since common ancestry or by the number of estimated speciation events separating taxa. However, apparent "punctuational" trait change can be recovered on molecular phylogenies if the rate of phenotypic evolution is correlated with the rate of speciation. Strong support for punctuational models can arise even if the underlying mode of trait evolution is strictly gradual, so long as rates of speciation and trait evolution covary across the branches of phylogenetic trees, and provided that lineages vary in their rate of speciation. Species selection for accelerated rates of ecological or phenotypic divergence can potentially lead to the perception that most trait divergence occurs in association with speciation events.     

Parallel genotypic adaptation: when evolution repeats itself

Until recently, parallel genotypic adaptation was considered unlikely because phenotypic differences were thought to be controlled by many genes. There is increasing evidence, however, that phenotypic variation sometimes has a simple genetic basis and that parallel adaptation at the genotypic level may be more frequent than previously believed. Here, we review evidence for parallel genotypic adaptation derived from a survey of the experimental evolution, phylogenetic, and quantitative genetic literature. The most convincing evidence of parallel genotypic adaptation comes from artificial selection experiments involving microbial populations. In some experiments, up to half of the nucleotide substitutions found in independent lineages under uniform selection are the same. Phylogenetic studies provide a means for studying parallel genotypic adaptation in non-experimental systems, but conclusive evidence may be difficult to obtain because homoplasy can arise for other reasons. Nonetheless, phylogenetic approaches have provided evidence of parallel genotypic adaptation across all taxonomic levels, not just microbes. Quantitative genetic approaches also suggest parallel genotypic evolution across both closely and distantly related taxa, but it is important to note that this approach cannot distinguish between parallel changes at homologous loci versus convergent changes at closely linked non-homologous loci. The finding that parallel genotypic adaptation appears to be frequent and occurs at all taxonomic levels has important implications for phylogenetic and evolutionary studies. With respect to phylogenetic analyses, parallel genotypic changes, if common, may result in faulty estimates of phylogenetic relationships. From an evolutionary perspective, the occurrence of parallel genotypic adaptation provides increasing support for determinism in evolution and may provide a partial explanation for how species with low levels of gene flow are held together.     

The place of phylogeny and cladistics in Evo-Devo research

Here we review the various uses to which phylogenetic trees may be put when analysing the evolution of organisms and of the genotypic and phenotypic characteristics of these organisms. We briefly discuss the cladistic method and its application in the inference of phylogenetictrees. Next we consider the uses to which phylogenetic trees can be put: in particular for determining the homology or otherwise of characters distributed on those trees and for estimating the likely characteristics of ancestral taxa. Finally we show the application of this information for deepening our understanding of the processes of evolution. All of these forms of inference are fundamental for comparative biology and of immediate importance to the practice of evolutionary developmental biology.     

Relatedness, phylogeny, and evolution of the fungi

Recent advances in fungal systematics are reviewed in relation to our previous studies. The usefulness of the integrated analysis of genotypic (especially 18S rRNA gene sequence comparisons) and phenotypic (especially ultrastructural and chemotaxonomic data) characters has been emphasized for the major groups and selected taxa of the fungi, and the impact to fungal systematics and evolution is discussed. Our noteworthy studies and findings are: 1) polyphyly of the chytridiomycetes and zygomycetes, 2) phylogenetic origin of the entomophthoralean fungi includingBasidiobolus, 3) detection of a major new lineage “Archiascomycetes,” comprisingTaphrina, Protomyces andSaitoella, Schizosaccharomyces, andPneumocystis, within the Ascomycota, and its phylogenetic and evolutionary significance, 4) polyphyletic origins of species in the anamorphic genusGeosmithia, and 5) phylogenetic placement ofMixia osmundae, species correctly and incorrectly assigned to the genusTaphrina, and basidiomyceotus yeasts. The newest 18S rDNA sequence-based neighbor-joining trees of the Ascomycota are demonstrated. “Traditional studies of evolution have amply demonstrated that evolution at the phenotypic level is characterized by adaptation and opportunism, irregularity in pace, and inequality of rates among lineages. In contrast, studies of molecular evolution have revealed quite different features characterized by changes that are conservative in nature, random in pattern (independent of phenotypic characters), and quite regular in pace with equal rates among diverge [sic] lineages for a given protein”. (Kimura, M. 1983. The neutral theory of molecular evolution, pp. 308–309, Cambridge University Press, Cambridge.) Recipient of the 2nd Mycological Society of Japan's Excellent Achievement Award, 1998; the awarding lecture was given at the 42nd Annual Meeting of the Mycological Society of Japan, 16 May, 1998, Kyoto University, Kyoto. This review is based mainly on the publications intended for the Award.     

Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.     

Testing the relationship between morphological and molecular rates of change along phylogenies

Abstract.— Molecular evolution has been considered to be essentially a stochastic process, little influenced by the pace of phenotypic change. This assumption was challenged by a study that demonstrated an association between rates of morphological and molecular change estimated for "total-evidence" phylogenies, a finding that led some researchers to challenge molecular date estimates of major evolutionary radiations. Here we show that Omland's (1997) result is probably due to methodological bias, particularly phylogenetic nonindependence, rather than being indicative of an underlying evolutionary phenomenon. We apply three new methods specifically designed to overcome phylogenetic bias to 13 published phylogenetic datasets for vertebrate taxa, each of which includes both morphological characters and DNA sequence data. We find no evidence of an association between rates of molecular and morphological rates of change.     

Positive correlations between molecular and morphological rates of evolution

The existence of positive associations between rates of molecular and morphological evolution (calculated from branch lengths of phylogenetic trees reconstructed using molecular and morphological characters, respectively) is important to issues of neutrality in sequence evolution, phylogenetic reconstructions assuming neutrality, and evolutionary genotype-phenotype mapping. Rates correlate positively when including branches leading to extant species (tips). Excluding tips, trends are similar, but statistical significances decrease systematically. This is due to (a) lower statistical power (excluding tips reduces sample sizes), and (b) rates are solely calculated from inaccurately reconstructed character states of extinct ancestral species, and this noise decreases correlation strengths. Correlations between molecular and morphological rates of evolution increase as more morphological characters are included for phylogenetic reconstruction. Sequence lengths apparently affect correlations along similar principles. Analyses of plant phylogenies confirm those from animals: sampling biases decrease correlations between molecular and morphological rates of evolution. Results confirm that genotype and phenotype are linked, and suggest adaptive components for molecular evolution. The discussion stresses the difficulties associated with analyses and conclusions based on data deduced from phylogenetic reconstruction.     

Understanding phylogenetic incongruence: lessons from phyllostomid bats

All characters and trait systems in an organism share a common evolutionary history that can be estimated using phylogenetic methods. However, differential rates of change and the evolutionary mechanisms driving those rates result in pervasive phylogenetic conflict. These drivers need to be uncovered because mismatches between evolutionary processes and phylogenetic models can lead to high confidence in incorrect hypotheses. Incongruence between phylogenies derived from morphological versus molecular analyses, and between trees based on different subsets of molecular sequences has become pervasive as datasets have expanded rapidly in both characters and species. For more than a decade, evolutionary relationships among members of the New World bat family Phyllostomidae inferred from morphological and molecular data have been in conflict. Here, we develop and apply methods to minimize systematic biases, uncover the biological mechanisms underlying phylogenetic conflict, and outline data requirements for future phylogenomic and morphological data collection. We introduce new morphological data for phyllostomids and outgroups and expand previous molecular analyses to eliminate methodological sources of phylogenetic conflict such as taxonomic sampling, sparse character sampling, or use of different algorithms to estimate the phylogeny. We also evaluate the impact of biological sources of conflict: saturation in morphological changes and molecular substitutions, and other processes that result in incongruent trees, including convergent morphological and molecular evolution. Methodological sources of incongruence play some role in generating phylogenetic conflict, and are relatively easy to eliminate by matching taxa, collecting more characters, and applying the same algorithms to optimize phylogeny. The evolutionary patterns uncovered are consistent with multiple biological sources of conflict, including saturation in morphological and molecular changes, adaptive morphological convergence among nectar‐feeding lineages, and incongruent gene trees. Applying methods to account for nucleotide sequence saturation reduces, but does not completely eliminate, phylogenetic conflict. We ruled out paralogy, lateral gene transfer, and poor taxon sampling and outgroup choices among the processes leading to incongruent gene trees in phyllostomid bats. Uncovering and countering the possible effects of introgression and lineage sorting of ancestral polymorphism on gene trees will require great leaps in genomic and allelic sequencing in this species‐rich mammalian family. We also found evidence for adaptive molecular evolution leading to convergence in mitochondrial proteins among nectar‐feeding lineages. In conclusion, the biological processes that generate phylogenetic conflict are ubiquitous, and overcoming incongruence requires better models and more data than have been collected even in well‐studied organisms such as phyllostomid bats.     

Diversification on an ecologically constrained adaptive landscape

We used phylogenetic analysis of body-size ecomorphs in a crustacean species complex to gain insight into how spatial complexity of ecological processes generates and maintains biological diversity. Studies of geographically widespread species of Hyalella amphipods show that phenotypic evolution is tightly constrained in a manner consistent with adaptive responses to alternative predation regimes. A molecular phylogeny indicates that evolution of Hyalella ecomorphs is characterized by parallel evolution and by phenotypic stasis despite substantial levels of underlying molecular change. The phylogeny suggests that species diversification sometimes occurs by niche shifts, and sometimes occurs without a change in niche. Moreover, diversification in the Hyalella ecomorphs has involved the repeated evolution of similar phenotypic forms that exist in similar ecological settings, a hallmark of adaptive evolution. The evolutionary stasis observed in clades separated by substantial genetic divergence, but existing in similar habitats, is also suggestive of stabilizing natural selection acting to constrain phenotypic evolution within narrow bounds. We interpret the observed decoupling of genetic and phenotypic diversification in terms of adaptive radiation on an ecologically constrained adaptive landscape, and suggest that ecological constraints, perhaps acting together with genetic and functional constraints, may explain the parallel evolution and evolutionary stasis inferred by the phylogeny.     

METAMODELS AND PHYLOGENETIC REPLICATION: A SYSTEMATIC APPROACH TO THE EVOLUTION OF DEVELOPMENTAL PATHWAYS

Molecular genetic analysis of phenotypic variation has revealed many examples of evolutionary change in the developmental pathways that control plant and animal morphology. A major challenge is to integrate the information from diverse organisms and traits to understand the general patterns of developmental evolution. This integration can be facilitated by evolutionary metamodels—traits that have undergone multiple independent changes in different species and whose development is controlled by well-studied regulatory pathways. The metamodel approach provides the comparative equivalent of experimental replication, allowing us to test whether the evolution of each developmental pathway follows a consistent pattern, and whether different pathways are predisposed to different modes of evolution by their intrinsic organization. A review of several metamodels suggests that the structure of developmental pathways may bias the genetic basis of phenotypic evolution, and highlights phylogenetic replication as a value-added approach that produces deeper insights into the mechanisms of evolution than single-species analyses.     

Plant domestication slows pest evolution

Agricultural practices such as breeding resistant varieties and pesticide use can cause rapid evolution of pest species, but it remains unknown how plant domestication itself impacts pest contemporary evolution. Using experimental evolution on a comparative phylogenetic scale, we compared the evolutionary dynamics of a globally important economic pest – the green peach aphid (Myzus persicae) – growing on 34 plant taxa, represented by 17 crop species and their wild relatives. Domestication slowed aphid evolution by 13.5%, maintained 10.4% greater aphid genotypic diversity and 5.6% higher genotypic richness. The direction of evolution (i.e. which genotypes increased in frequency) differed among independent domestication events but was correlated with specific plant traits. Individual‐based simulation models suggested that domestication affects aphid evolution directly by reducing the strength of selection and indirectly by increasing aphid density and thus weakening genetic drift. Our results suggest that phenotypic changes during domestication can alter pest evolutionary dynamics.     

Artifactual phylogenies caused by correlated distribution of substitution rates among sites and lineages: the good, the bad, and the ugly

Despite the advances in understanding molecular evolution, current phylogenetic methods barely take account of a fraction of the complexity of evolution. We are chiefly constrained by our incomplete knowledge of molecular evolutionary processes and the limits of computational power. These limitations lead to the establishment of either biologically simplistic models that rarely account for a fraction of the complexity involved or overfitting models that add little resolution to the problem. Such oversimplified models may lead us to assign high confidence to an incorrect tree (inconsistency). Rate-across-site (RAS) models are commonly used evolutionary models in phylogenetic studies. These account for heterogeneity in the evolutionary rates among sites but do not account for changing within-site rates across lineages (heterotachy). If heterotachy is common, using RAS models may lead to systematic errors in tree inference. In this work we show possible misleading effects in tree inference when the assumption of constant within-site rates across lineages is violated using maximum likelihood. Using a simulation study, we explore the ways in which gamma stationary models can lead to wrong topology or to deceptive bootstrap support values when the within-site rates change across lineages. More precisely, we show that different degrees of heterotachy mislead phylogenetic inference when the model assumed is stationary. Finally, we propose a geometry-based approach to visualize and to test for the possible existence of bias due to heterotachy.     

Molecular phylogeny of plethodonine salamanders and hylid frogs: statistical analysis of protein comparisons.

The bootstrapping method of determining confidence in the topology of phylogenetic trees has been applied to electrophoretic protein data for two groups of amphibians: salamanders of two North American genera (Aneides and Plethodon) of the tribe Plethodontini and Holarctic hylid frogs. Some current methods of phylogenetic reconstruction for electrophoretic protein data have been evaluated by comparing the trees obtained from molecular data sets with available morphological data. Molecular data on the phylogenetic relationships of Aneides and Plethodon, data obtained from electrophoretic and immunological studies, indicate that Aneides probably was derived from western Plethodon subsequent to the separation of eastern and western Plethodon. Thus Plethodon very likely is a paraphyletic genus. The extremely low rate of morphological evolution in Plethodon compared with that in Aneides causes difficulty in indicating their evolutionary relationships taxonomically because there are no synapomorphic morphological characters that define either eastern or western Plethodon, whereas there are several for the genus Aneides. Thus molecular data alone probably indicate the evolutionary relationships of the species in these genera. Highton and Larson's (1979) arrangement of species of Plethodon into eight species groups is supported. The topologies of the unweighted pair-group method using arithmetic means (UPGMA) and distance Wagner trees were compared with independent morphological and molecular data on the relationships of the 28 plethodonine species. It was found that UPGMA trees indicate relationships that are more in agreement with other information than are those provided by distance Wagner trees. The use of the bootstrap technique indicates that the topologies of UPGMA trees are better supported statistically than are the topologies of distance Wagner trees. Moreover, different addition criteria produce a variety of distance Wagner trees with different topologies, each with several groupings that are not supported statistically. It is concluded that considerable caution should be used in interpreting the topology of distance Wagner trees. Very similar results were obtained with a second data set on 30 taxa of Holarctic hylid frogs. Trees obtained by the neighbor-joining method are more in agreement with UPGMA phenograms and other data, so this method of phylogenetic reconstruction may be useful to systematists not willing to assume constant rates of evolution.(ABSTRACT TRUNCATED AT 400 WORDS)     

Distinguishing coevolution from covicariance in an obligate pollination mutualism: asynchronous divergence in Joshua tree and its pollinators

Obligate pollination mutualisms--in which both plants and their pollinators are reliant upon one another for reproduction--represent some of the most remarkable coevolutionary interactions in the natural world. The intimacy and specificity of these interactions have led to the prediction that the plants and their pollinators may be prone to cospeciation driven by coevolution. Several studies have identified patterns of phylogenetic congruence that are consistent with this prediction, but it is difficult to determine the evolutionary process that underlies these patterns. Phylogenetic congruence might also be produced by extrinsic factors, such as a shared biogeographic history. We examine the biogeographic history of a putative case of codivergence in the obligate pollination mutualism between Joshua trees (Yucca brevifolia) and two sister species of pollinating yucca moths (Tegeticula spp.) We employ molecular phylogenetic methods and coalescent-based approaches, in combination with relaxed-clock estimates of absolute rates of molecular evolution, to analyze multi-locus sequence data from more than 30 populations of Y. brevifolia and its pollinators. The results indicate that the moth species diverged significantly (p < 0.01) more recently than their corresponding host populations, suggesting that the apparent codivergence is not an artifact of a shared biogeographic history.     

What invasive species reveal about the rate and form of contemporary phenotypic change in nature

Biological invasions are opportunities to gain insight into fundamental evolutionary questions, because reproductive isolation and sudden alterations in selection pressures are likely to lead to rapid evolutionary change. Here I investigate the role played by invasive species in revealing the rate and form of contemporary phenotypic change in wild populations by expanding a database of more than 5,500 rates of phenotypic change from 90 species of plants and animals. Invasive species are frequently used as model organisms and thus contribute disproportionately to available rates of phenotypic change. However, the preponderance of these rates is the consequence of extensive study in a small number of species. I found mixed evidence to support the hypothesis that phenotypic change is associated with time depending on the metric of choice (i.e., darwins or haldanes). Insights from both invasive and native species provide evidence for abrupt phenotypic change and suggest that the environment plays a potentially important role in driving trait change in wild populations, although the environmental influence on the observed trajectories remains unclear. Thus, future work should continue to seek an understanding of the mechanistic underpinnings--both genetic and environmental--of how phenotypic variation allows populations to adapt to rapidly changing global environments.     

When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model

Conceptual models of adaptive radiation predict that competitive interactions among species will result in an early burst of speciation and trait evolution followed by a slowdown in diversification rates. Empirical studies often show early accumulation of lineages in phylogenetic trees, but usually fail to detect early bursts of phenotypic evolution. We use an evolutionary simulation model to assemble food webs through adaptive radiation, and examine patterns in the resulting phylogenetic trees and species' traits (body size and trophic position). We find that when foraging trade-offs result in food webs where all species occupy integer trophic levels, lineage diversity and trait disparity are concentrated early in the tree, consistent with the early burst model. In contrast, in food webs in which many omnivorous species feed at multiple trophic levels, high levels of turnover of species' identities and traits tend to eliminate the early burst signal. These results suggest testable predictions about how the niche structure of ecological communities may be reflected by macroevolutionary patterns.     

BioEssays 10/2020

Frequent independent origins of environmental sex determination (ESD) are assumed within amniotes. However, the phylogenetic distribution of sex-determining modes suggests that ESD is likely very ancient and may be homologous across ESD groups. Sex chromosomes are demonstrated to be old and stable in endothermic (mammals and birds) and many ectothermic (non-avian reptiles) lineages, but they are mostly non-homologous between individual amniote lineages. The phylogenetic pattern may be explained by ancestral ESD with multiple transitions to later evolutionary stable genotypic sex determination. It is pointed out here that amniote ESD shares several key aspects with sequential hermaphroditism of fishes such as a lack of sex differences in genomes, biased population sex ratios, and potentially also molecular mechanism related to general stress responses. Here, it is speculated that ESD evolves via a heterochronic shift of the sensitive period of sex change from the adult to the embryonic stage in a hermaphroditic amniote ancestor. Also see the video abstract here https://youtu.be/q2mjtlCefu4 .     

From genotype to phenotype: buffering mechanisms and the storage of genetic information

DNA sequence variation is abundant in wild populations. While molecular biologists use genetically homogeneous strains of model organisms to avoid this variation, evolutionary biologists embrace genetic variation as the material of evolution since heritable differences in fitness drive evolutionary change. Yet, the relationship between the phenotypic variation affecting fitness and the genotypic variation producing it is complex. Genetic buffering mechanisms modify this relationship by concealing the effects of genetic and environmental variation on phenotype. Genetic buffering allows the build-up and storage of genetic variation in phenotypically normal populations. When buffering breaks down, thresholds governing the expression of previously silent variation are crossed. At these thresholds, phenotypic differences suddenly appear and are available for selection. Thus, buffering mechanisms modulate evolution and regulate a balance between evolutionary stasis and change. Recent work provides a glimpse of the molecular details governing some types of genetic buffering.     

Molecular Phylogeny and Coevolution

Abstract Recent advances in molecular phylogenetic estimation in diverse organisms have improved our understanding of coevolution. From the phylogenies of interacting organisms, we can interpret the evolution of adaptive characters, and the history of interaction. Molecular approaches are generally more informative than these based solely on phenotypic characters. Molecular genetic method can be applied to organisms that have only simple morphological features and can be used for comparisons at any taxonomic level. Estimation of divergence time is also possible but still difficult because evolutionary rates of macromolecules are not always constant and suitable fossil records are often not available for calibrating rates of change. Here I review recent progress in the application of molecular techniques to the interpretation of coevolutionary relationships.     

克隆植物的表型可塑性与等级选择

表型可塑性是指生物个体生长发育过程中遭受不同环境条件作用时产生不同表型的能力。进化的发生有赖于自然选择对种群遗传可变性产生的效力以及各基因型的表型可塑性。有足够的证据说明表型可塑性的可遗传性,它实际上是进化改变的一个成分。一般通过优化模型、数量遗传模型和配子模型来研究表型可塑性的进化。植物的构型是相对固定的,并未完全抑制表型可塑性。克隆植物因其双构件性而具有更广泛的、具有重要生态适应意义的表型可塑性。构件性使克隆植物具有以分株为基本单位的等级结构,从而使克隆植物的表型选择也具有等级性。构件等级一般包含基株、克隆片段或分株系统以及分株3个典型水平。目前认为克隆植物的自然选择有两种模式,分别以等级选择模型和基因型选择模型表征。等级选择模型认为:不同的等级水平同时也是表型选择水平,环境对各水平具有作用,各水平之间也有相互作用,多重表型选择水平的净效应最终通过繁殖水平——分株传递到随后的世代中。基因型选择模型指出:克隆生长引起分株的遗传变异,并通过基株内分株间以及基株间的非随机交配引起种子库等位基因频率的改变,产生微进化。这两种选择模式均突出强调了分株水平在自然选择过程中的变异性以及在进化中的重要性,强调了克隆生长和种子繁殖对基株适合度的贡献。基因型选择模型包含等级选择模型的观点,是对等级选择模型的重要补充。克隆植物的表型可塑性表现在3个典型等级层次上,由于各层次对自然选择压力具有不同的反应,其表型变异程度一般表现出“分株层次>分株片段层次>基株层次”的等级性反应模式。很多证据表明,在构件有机体中构件具有最大的表型可塑性,植物的表型可塑性实际上是构件而非整个遗传个体的反应。这说明克隆植物的等级反应模式可能具有普适性。如果该反应模式同时还是构件等级中不同“个体”适应性可塑性反应的模式,那么可以预测:1)在克隆植物中,分株层次受到的自然选择强度也最大,并首先发生适应性可塑性变化,最终引起克隆植物微进化;2)由于较弱的有性繁殖能力,克隆植物在进化过程中的保守性可能大于非克隆植物。克隆植物等级反应模式的普适性亟待验证。