Macroevolution is more than repeated rounds of microevolution

SUMMARY Arguments over macroevolution versus microevolution have waxed and waned through most of the twentieth century. Initially, paleontologists and other evolutionary biologists advanced a variety of non-Darwinian evolutionary processes as explanations for patterns found in the fossil record, emphasizing macroevolution as a source of morphologic novelty. Later, paleontologists, from Simpson to Gould, Stanley, and others, accepted the primacy of natural selection but argued that rapid speciation produced a discontinuity between micro- and macroevolution. This second phase emphasizes the sorting of innovations between species. Other discontinuities appear in the persistence of trends (differential success of species within clades), including species sorting, in the differential success between clades and in the origination and establishment of evolutionary novelties. These discontinuities impose a hierarchical structure to evolution and discredit any smooth extrapolation from allelic substitution to large-scale evolutionary patterns. Recent developments in comparative developmental biology suggest a need to reconsider the possibility that some macroevolutionary discontinuites may be associated with the origination of evolutionary innovation. The attractiveness of macroevolution reflects the exhaustive documentation of large-scale patterns which reveal a richness to evolution unexplained by microevolution. If the goal of evolutionary biology is to understand the history of life, rather than simply document experimental analysis of evolution, studies from paleontology, phylogenetics, developmental biology, and other fields demand the deeper view provided by macroevolution.     

SPECIES SELECTION AND THE MACROEVOLUTION OF CORAL COLONIALITY AND PHOTOSYMBIOSIS

Differences in the relative diversification rates of species with variant traits are known as species selection. Species selection can produce a macroevolutionary change in the frequencies of traits by changing the relative number of species possessing each trait over time. But species selection is not the only process that can change the frequencies of traits, phyletic microevolution of traits within species and phylogenetic trait evolution among species, the tempo and mode of microevolution can also change trait frequencies. Species selection, phylogenetic, and phyletic processes can all contribute to large‐scale trends, reinforcing or canceling each other out. Even more complex interactions among macroevolutionary processes are possible when multiple covarying traits are involved. Here I present a multilevel macroevolutionary framework that is useful for understanding how macroevolutionary processes interact. It is useful for empirical studies using fossils, molecular phylogenies, or both. I illustrate the framework with the macroevolution of coloniality and photosymbiosis in scleractinian corals using a time‐calibrated molecular phylogeny. I find that standing phylogenetic variation in coloniality and photosymbiosis deflects the direction of macroevolution from the vector of species selection. Variation in these traits constrains species selection and results in a 200 million year macroevolutionary equilibrium.     

What is macroevolution?

Definitions of macroevolution fall into three categories: (1) evolution of taxa of supraspecific rank; (2) evolution on the grand time-scale; and (3) evolution that is guided by sorting of interspecific variation (as opposed to sorting of intraspecific variation in microevolution). Here, it is argued that only definition 3 allows for a consistent separation of macroevolution and microevolution. Using this definition, speciation has both microevolutionary and macroevolutionary aspects: the process of morphological transformation is microevolutionary, but the variation among species that it produces is macroevolutionary, as is the rate at which speciation occurs. Selective agents may have differential effects on intraspecific and interspecific variation, with three possible situations: effect at one level only, effect at both levels with the same polarity but potentially different intensity, and effects that oppose between levels. Whereas the impact of all selective agents is direct in macroevolution, microevolution requires intraspecific competition as a mediator between selective agents and evolutionary responses. This mediating role of intraspecific competition occurs in the presence of sexual reproduction and has therefore no analogue at the macroevolutionary level where species are the evolutionary units. Competition between species manifests both on the microevolutionary and macroevolutionary level, but with different effects. In microevolution, interspecific competition spurs evolutionary divergence, whereas it is a potential driver of extinction at the macroevolutionary level. Recasting the Red Queen hypothesis in a macroevolutionary framework suggests that the effects of interspecific competition result in a positive correlation between origination and extinction rates, confirming empirical observations herein referred to as Stanley's rule.     

Developmental bias,macroevolution, and the fossil record

A fuller understanding of the role of developmental bias in shaping large‐scale evolutionary patterns requires integrating bias (the probability distribution of variation accessible to an ancestral phenotype) with clade dynamics (the differential survival and production of species and evolutionary lineages). This synthesis could proceed as a two‐way exchange between the developmental data available to neontologists and the strictly phenotypic but richly historical and dynamic data available to paleontologists. Analyses starting in extant populations could aim to predict macroevolution in the fossil record from observed developmental bias, while analyses starting in the fossil record, particularly the record of extant species and lineages, could aim to predict developmental bias from macroevolutionary patterns, including the broad range of extinct phenotypes. Analyses in multivariate morphospaces are especially effective when coupled with phylogeny, theoretical and developmental models, and diversity–disparity plots. This research program will also require assessing the “heritability” of an ancestral bias across phylogeny, and the tendency for bias change in strength and orientation over evolutionary time. Such analyses will help find a set of general rules for the macroevolutionary effects of developmental bias, including its impact on and interactions with the other intrinsic and extrinsic factors governing the movement, expansion, and contraction of clades in morphospace.     

The Developmental Basis of Variational Modularity: Insights from Quantitative Genetics,Morphometrics, and Developmental Biology

Groups of correlated characters (variational modules) often are considered to be the result of dissociated local developmental factors, i.e., of a modular genotype–phenotype map. But certain sets of pleiotropic factors can equally well induce modular phenotypic variation—no local developmental factors are necessary for a modular covariance structure. It is thus not possible to infer genetic or developmental modularity from standing variation alone. Yet, only for approximately linear genotype–phenotype maps is the induced covariance structure stable over changes of the phenotypic mean. For larger genetic and phenotypic variation, such as on a macroevolutionary level, developmental effects often are nonlinear and variational modularity remains stable only when it is realized by local dissociated developmental factors with no overlap of pleiotropic ranges. The evo-devo concept of modularity concurs only at this macroevolutionary level with the quantitative notion of variational modularity. Empirical evidence on the genetic and developmental architecture underlying phenotypic variation is inconclusive and partly subject to methodological problems. Many studies seem to indicate modularized phenotypic variation and local clusters of QTL effects, whereas other studies find support for several alternative models of modularity and report continuous distributions of QTL effects. This inconsistency partly results from the neglect of spatial relationships among the measured traits. Given the complex development of higher organisms, a combination of pleiotropic factors and more local developmental effects with a hierarchical, overlapping, and more or less continuous distribution appears most likely.     

SCALE AND HIERARCHY IN MACROEVOLUTION

Abstract: Scale and hierarchy must be incorporated into any conceptual framework for the study of macroevolution, i.e. evolution above the species level. Expansion of temporal and spatial scales reveals evolutionary patterns and processes that are virtually inaccessible to, and unpredictable from, short‐term, localized observations. These larger‐scale phenomena range from evolutionary stasis at the species level and the mosaic assembly of complex morphologies in ancestral forms to the non‐random distribution in time and space of the origin of major evolutionary novelties, as exemplified by the Cambrian explosion and post‐extinction recoveries of metazoans, and the preferential origin of major marine groups in onshore environments and tropical waters. Virtually all of these phenomena probably involve both ecological and developmental factors, but the integration of these components with macroevolutionary theory has only just begun. Differential survival and reproduction of units can occur at several levels within a biological hierarchy that includes DNA sequences, organisms, species and clades. Evolution by natural selection can occur at any level where there is heritable variation that affects birth and death of units by virtue of interaction with the environment. This dynamic can occur when selfish DNA sequences replicate disproportionately within genomes, when organisms enjoy fitness advantages within populations (classical Darwinian selection), when differential speciation or extinction occurs within clades owing to organismic properties (effect macroevolution), and when differential speciation or extinction occurs within clades owing to emergent, species‐level properties (in the strict sense species selection). Operationally, emergent species‐level properties such as geographical range can be recognized by testing whether their macroevolutionary effects are similar regardless of the different lower‐level factors that produce them. Large‐scale evolutionary trends can be driven by transformation of species, preferential production of species in a given direction, differential origination or extinction, or any combination of these; the potential for organismic traits to hitch‐hike on other factors that promote speciation or damp extinction is high. Additional key attributes of macroevolutionary dynamics within biological hierarchies are that (1) hierarchical levels are linked by upward and downward causation, so that emergent properties at a focal level do not impart complete independence; (2) hierarchical effects are asymmetrical, so that dynamics at a given focal level need not propagate upwards, but will always cascade downwards; and (3) rates are generally, although not always, faster at lower hierarchical levels. Temporal and spatial patterns in the origin of major novelties and higher taxa are significantly discordant from those at the species and genus levels, suggesting complex hierarchical effects that remain poorly understood. Not only are many of the features promoting survivorship during background times ineffective during mass extinctions, but also they are replaced in at least some cases by higher‐level, irreducible attributes such as clade‐level geographical range. The incorporation of processes that operate across hierarchical levels and a range of temporal and spatial scales has expanded and enriched our understanding of evolution.     

Range margin populations show high climate adaptation lags in European trees

How populations of long‐living species respond to climate change depends on phenotypic plasticity and local adaptation processes. Marginal populations are expected to have lags in adaptation (i.e. differences between the climatic optimum that maximizes population fitness and the local climate) because they receive pre‐adapted alleles from core populations preventing them from reaching a local optimum in their climatically marginal habitat. Yet, whether adaptation lags in marginal populations are a common feature across phylogenetically and ecologically different species and how lags can change with climate change remain unexplored. To test for range‐wide patterns of phenotypic variation and adaptation lags of populations to climate, we (a) built model ensembles of tree height accounting for the climate of population origin and the climate of the site for 706 populations monitored in 97 common garden experiments covering the range of six European forest tree species; (b) estimated populations' adaptation lags as the differences between the climatic optimum that maximizes tree height and the climate of the origin of each population; (c) identified adaptation lag patterns for populations coming from the warm/dry and cold/wet margins and from the distribution core of each species range. We found that (a) phenotypic variation is driven by either temperature or precipitation; (b) adaptation lags are consistently higher in climatic margin populations (cold/warm, dry/wet) than in core populations; (c) predictions for future warmer climates suggest adaptation lags would decrease in cold margin populations, slightly increasing tree height, while adaptation lags would increase in core and warm margin populations, sharply decreasing tree height. Our results suggest that warm margin populations are the most vulnerable to climate change, but understanding how these populations can cope with future climates depend on whether other fitness‐related traits could show similar adaptation lag patterns.     

Song evolution,speciation, and vocal learning in passerine birds

Phenotypic divergence can promote reproductive isolation and speciation, suggesting a possible link between rates of phenotypic evolution and the tempo of speciation at multiple evolutionary scales. To date, most macroevolutionary studies of diversification have focused on morphological traits, whereas behavioral traits─including vocal signals─are rarely considered. Thus, although behavioral traits often mediate mate choice and gene flow, we have a limited understanding of how behavioral evolution contributes to diversification. Furthermore, the developmental mode by which behavioral traits are acquired may affect rates of behavioral evolution, although this hypothesis is seldom tested in a phylogenetic framework. Here, we examine evidence for rate shifts in vocal evolution and speciation across two major radiations of codistributed passerines: one oscine clade with learned songs (Thraupidae) and one suboscine clade with innate songs (Furnariidae). We find that evolutionary bursts in rates of speciation and song evolution are coincident in both thraupids and furnariids. Further, overall rates of vocal evolution are higher among taxa with learned rather than innate songs. Taken together, these findings suggest an association between macroevolutionary bursts in speciation and vocal evolution, and that the tempo of behavioral evolution can be influenced by variation in developmental modes among lineages.     

IS MACROEVOLUTION MORE THAN SUCCESSIVE ROUNDS OF MICROEVOLUTION?

Abstract:  Whether macrovolution is reducible to microevolution is one of the persistent debates in evolutionary biology. Although the concept of emergence is important to answering this question, it has not been extensively discussed within palaeobiology. A taxonomy of emergence concepts is presented to clarify the ways in which emergence relates to this debate. Weak emergence is a particularly helpful way to understand the hierarchical nature of biology: it captures the ways in which higher-level traits depend on lower-level processes, while recognizing that emergent traits can nonetheless provide the basis for autonomous higher-level theories. A brief review of the biological literature suggests that geographical range size is weakly emergent. While some concepts of emergence do not block the attempt to reduce macroevolution (i.e. the attempt to explain all macroevolutionary phenomena in terms of microevolutionary processes), weak emergence does. Thus, if geographical range is weakly emergent, it provides a basis for arguing that macroevolutionary phenomena cannot be fully explained by microevolutionary processes.     

Evolutionary divergence in directions of high phenotypic variance in the ostracode genus poseidonamicus

Trait variation and covariation are understood to influence the response of populations to natural selection on generational time scales, but their role, if any, in shaping long-term macroevolutionary divergence is still unclear. The present study uses the rich fossil record of the ostracode genus Poseidonamicus to reconstruct in great detail the evolutionary history of a set of landmark-based morphometric characters. This reconstruction included two kinds of evolutionary inferences: ancestor-descendant transitions among populations repeatedly sampled at the same location and divergence between lineages measured as independent contrasts on a phylogeny. This reconstructed history was then used to test if evolutionary changes were concentrated in directions (traits or combinations of traits) with high phenotypic variance. Two different statistics of association between evolution and variation tested the null hypothesis that evolutionary changes occur in random directions with respect to trait variability. The first of these measured the similarity between the directions of evolutionary change and the axis of maximum variance, and the second measured the degree to which evolutionary changes were concentrated in directions of high phenotypic variation. Randomization tests indicated that both kinds of evolutionary inferences (ancestor-descendant and phylogenetic contrasts) occurred preferentially in directions of high phenotypic variance (and close to the axis of maximal variation), suggesting that within-population variation can structure long-term divergence. This effect decayed after a few million years, but at least for one metric, never disappeared completely. These results are consistent with Schluter's genetic constraints model in which evolutionary trajectories on adaptive landscapes are deflected by variation within and covariation among traits.     

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.     

Ecological and evolutionary drivers of range size in Coenagrion damselflies

Geographic range size is a key ecological and evolutionary characteristic of a species, yet the causal basis of variation in range size among species remains largely unresolved. One major reason for this is that several ecological and evolutionary traits may jointly shape species' differences in range size. We here present an integrated study of the contribution of ecological (dispersal capacity, body size and latitudinal position) and macroevolutionary (species' age) traits in shaping variation in species' range size in Coenagrion damselflies. We reconstructed the phylogenetic tree of this genus to account for evolutionary history when assessing the contribution of the ecological traits and to evaluate the role of the macroevolutionary trait (species' age). The genus invaded the Nearctic twice independently from the Palearctic, yet this was not associated with the evolution of larger range sizes or dispersal capacity. Body size and species' age did not explain variation in range size. There is higher flight ability (as measured by wing aspect ratio) at higher latitudes. Species with a larger wing aspect ratio had a larger range size, also after correcting for phylogeny, suggesting a role for dispersal capacity in shaping the species' ranges. More northern species had a larger species' range, consistent with Rapoport's rule, possibly related to niche width. Our results underscore the importance of integrating macroecology and macroevolution when explaining range size variation among species.     

The importance of protistan phylogeny for macroevolution

Explicit estimates of protist phylogeny should play a key role in the development of macroevolutionary theory. Nearly half the evolutionary history of living systems involved only protists, and many trends and traits of macroevolutionary significance originated in protist groups. Special areas of research that can make use of protist phylogenies include: (1) origin of life studies, (2) biotic aspects of the evolution of the environment, (3) developmental biology and evolution, and (4) macroevolutionary trends in the diversification of life.     

A conceptual framework of evolutionary novelty and innovation

Since 1990 the recognition of deep homologies among metazoan developmental processes and the spread of more mechanistic approaches to developmental biology have led to a resurgence of interest in evolutionary novelty and innovation. Other evolutionary biologists have proposed central roles for behaviour and phenotypic plasticity in generating the conditions for the construction of novel morphologies, or invoked the accessibility of new regions of vast sequence spaces. These approaches contrast with more traditional emphasis on the exploitation of ecological opportunities as the primary source of novelty. This definitional cornucopia reflects differing stress placed on three attributes of novelties: their radical nature, the generation of new taxa, and ecological and evolutionary impact. Such different emphasis has led to conflating four distinct issues: the origin of novel attributes (genes, developmental processes, phenotypic characters), new functions, higher clades and the ecological impact of new structures and functions. Here I distinguish novelty (the origin of new characters, deep character transformations, or new combinations) from innovation, the ecological and evolutionary success of clades. Evidence from the fossil record of macroevolutionary lags between the origin of a novelty and its ecological success demonstrates that novelty may be decoupled from innovation, and only definitions of novelty based on radicality (rather than generativity or consequentiality) can be assessed without reference to the subsequent history of the clade to which a novelty belongs. These considerations suggest a conceptual framework for novelty and innovation, involving: (i) generation of the potential for novelty; (ii) the formation of novel attributes; (iii) refinement of novelties through adaptation; (iv) exploitation of novelties by a clade, which may coincide with a new round of ecological or environmental potentiation; followed by (v) the establishment of innovations through ecological processes. This framework recognizes that there is little empirical support for either the dominance of ecological opportunity, nor abrupt discontinuities (often caricatured as ‘hopeful monsters’). This general framework may be extended to aspects of cultural and social innovation.     

Macroevolution of arboreality in salamanders

Evolutionary theory predicts that selection in distinct microhabitats generates correlations between morphological and ecological traits, and may increase both phenotypic and taxonomic diversity. However, some microhabitats exert unique selective pressures that act as a restraining force on macroevolutionary patterns of diversification. In this study, we use phylogenetic comparative methods to investigate the evolutionary outcomes of inhabiting the arboreal microhabitat in salamanders. We find that arboreality has independently evolved at least five times in Caudata and has arisen primarily from terrestrial ancestors. However, the rate of transition from arboreality back to terrestriality is 24 times higher than the converse. This suggests that macroevolutionary trends in microhabitat use tend toward terrestriality over arboreality, which influences the extent to which use of the arboreal microhabitat proliferates. Morphologically, we find no evidence for an arboreal phenotype in overall body proportions or in foot shape, as variation in both traits overlaps broadly with species that utilize different microhabitats. However, both body shape and foot shape display reduced rates of phenotypic evolution in arboreal taxa, and evidence of morphological convergence among arboreal lineages is observed. Taken together, these patterns suggest that arboreality has played a unique role in the evolution of this family, providing neither an evolutionary opportunity, nor an evolutionary dead end.     

Does phenotypic plasticity initiate developmental bias?

The generation of variation is paramount for the action of natural selection. Although biologists are now moving beyond the idea that random mutation provides the sole source of variation for adaptive evolution, we still assume that variation occurs randomly. In this review, we discuss an alternative view for how phenotypic plasticity, which has become well accepted as a source of phenotypic variation within evolutionary biology, can generate nonrandom variation. Although phenotypic plasticity is often defined as a property of a genotype, we argue that it needs to be considered more explicitly as a property of developmental systems involving more than the genotype. We provide examples of where plasticity could be initiating developmental bias, either through direct active responses to similar stimuli across populations or as the result of programmed variation within developmental systems. Such biased variation can echo past adaptations that reflect the evolutionary history of a lineage but can also serve to initiate evolution when environments change. Such adaptive programs can remain latent for millions of years and allow development to harbor an array of complex adaptations that can initiate new bouts of evolution. Specifically, we address how ideas such as the flexible stem hypothesis and cryptic genetic variation overlap, how modularity among traits can direct the outcomes of plasticity, and how the structure of developmental signaling pathways is limited to a few outcomes. We highlight key questions throughout and conclude by providing suggestions for future research that can address how plasticity initiates and harbors developmental bias.     

Speciation and development

Understanding general principles about the origin of species remains one of the foundational challenges in evolutionary biology. The genomic divergence between groups of individuals can spawn hybrid inviability and hybrid sterility, which presents a tantalizing developmental problem. Divergent developmental programs may yield either conserved or divergent phenotypes relative to ancestral traits, both of which can be responsible for reproductive isolation during the speciation process. The genetic mechanisms of developmental evolution involve cis- and trans-acting gene regulatory change, protein–protein interactions, genetic network structures, dosage, and epigenetic regulation, all of which also have roots in population genetic and molecular evolutionary processes. Toward the goal of demystifying Darwin's “mystery of mysteries,” this review integrates microevolutionary concepts of genetic change with principles of organismal development, establishing explicit links between population genetic process and developmental mechanisms in the production of macroevolutionary pattern. This integration aims to establish a more unified view of speciation that binds process and mechanism.