Species selection and random drift in macroevolution

Species selection resulting from trait‐dependent speciation and extinction is increasingly recognized as an important mechanism of phenotypic macroevolution. However, the recent bloom in statistical methods quantifying this process faces a scarcity of dynamical theory for their interpretation, notably regarding the relative contributions of deterministic versus stochastic evolutionary forces. I use simple diffusion approximations of birth‐death processes to investigate how the expected and random components of macroevolutionary change depend on phenotype‐dependent speciation and extinction rates, as can be estimated empirically. I show that the species selection coefficient for a binary trait, and selection differential for a quantitative trait, depend not only on differences in net diversification rates (speciation minus extinction), but also on differences in species turnover rates (speciation plus extinction), especially in small clades. The randomness in speciation and extinction events also produces a species‐level equivalent to random genetic drift, which is stronger for higher turnover rates. I then show how microevolutionary processes including mutation, organismic selection, and random genetic drift cause state transitions at the species level, allowing comparison of evolutionary forces across levels. A key parameter that would be needed to apply this theory is the distribution and rate of origination of new optimum phenotypes along a phylogeny.     

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.     

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.     

Competition and macroevolution: the ghost of competition yet to come?

Competition theory is the focus of much debate among both neontologists and palaeontologists. This paper explores the expansion of competition theory into macroevolution, since this is the relevant context for palaeobiologists, and challenges the contention that microevolutionary processes are generally inappropriate to the interpretation of macroevolutionary pattern. We show that the term 'interspecific competition' is imprecise, since it conflates processes operating at various hierarchical levels, and recommend a terminological change in accordance with hierarchy theory. Finally, we reassess the role of competition and its absence in radiations. Since evolutionary novelties must be fixed at speciation, and speciation occurs in response to habitat destruction rather than the freeing of ecological space, we believe the role of competition to be minimal in both radiation and the generation of novelty.     

The continuity of microevolution and macroevolution

A persistent debate in evolutionary biology is one over the continuity of microevolution and macroevolution – whether macroevolutionary trends are governed by the principles of microevolution. The opposition of evolutionary trends over different time scales is taken as evidence that selection is uncoupled over these scales. I argue that the paradox inferred by trend opposition is eliminated by a hierarchical application of the ‘geometric‐mean fitness’ principle, a principle that has been invoked only within the limited context of microevolution in response to environmental variance. This principle implies the elimination of well adapted genotypes – even those with the highest arithmetic mean fitness over a shorter time scale. Contingent on premises concerning the temporal structure of environmental variance, selectivity of extinction, and clade‐level heritability, the evolutionary outcome of major environmental change may be viewed as identical in principle to the outcome of minor environmental fluctuations over the short‐term. Trend reversals are thus recognized as a fundamental property of selection operating at any phylogenetic level that occur in response to event severities of any magnitude over all time scales. This ‘bet‐hedging’ perspective differs from others in that a specified, single hierarchical selective process is proposed to explain observed hierarchical patterns of extinction.     

Biotic interactions and macroevolution: extensions and mismatches across scales and levels

Clade dynamics in the fossil record broadly fit expectations from the operation of competition, predation, and mutualism, but data from both modern and ancient systems suggest mismatches across scales and levels. Indirect effects, as when antagonistic or mutualistic interactions restrict geographic range and thereby elevate extinction risk, are probably widespread and may flow in both directions, as when species- or organismic-level factors increase extinction risk or speciation probabilities. Apparent contradictions across scales and levels have been neglected, including (1) the individualistic geographic shifts of species on centennial and millennial timescales versus evidence for fine-tuned coevolutionary relationships; (2) the extensive and dynamic networks of interactions faced by most species versus the evolution of costly enemy-specific defenses and finely attuned mutualisms; and (3) the macroevolutionary lags often seen between the origin and the diversification of a clade or an evolutionary novelty versus the rapid microevolution of advantageous phenotypes and the invasibility of most communities. Resolution of these and other cross-level tensions presumably hinges on how organismic interactions impinge on genetic population structures, geographic ranges, and the persistence of incipient species, but generalizations are not yet possible. Paleontological and neontological data are both incomplete and so the most powerful response to these problems will require novel integrative approaches. Promising research areas include more realistic approaches to modeling and empirical analysis of large-scale diversity dynamics of ostensibly competing clades; spatial and phylogenetic dissections of clades involved in escalatory dynamics (where prey respond evolutionarily to a broad and shifting array of enemies); analyses of the short- versus long-term consequences of mutualistic symbioses; and fuller use of abundant natural experiments on the evolutionary impacts of ecosystem engineers.     

Advancing the metabolic theory of biodiversity

A component of metabolic scaling theory has worked towards understanding the influence of metabolism over the generation and maintenance of biodiversity. Specific models within this ‘metabolic theory of biodiversity’ (MTB) have addressed temperature gradients in speciation rate and species richness, but the scope of MTB has been questioned because of empirical departures from model predictions. In this study, we first show that a generalized MTB is not inconsistent with empirical patterns and subsequently implement an eco‐evolutionary MTB which has thus far only been discussed qualitatively. More specifically, we combine a functional trait (body mass) approach and an environmental gradient (temperature) with a dynamic eco‐evolutionary model that builds on the current MTB. Our approach uniquely accounts for feedbacks between ecological interactions (size‐dependent competition and predation) and evolutionary rates (speciation and extinction). We investigate a simple example in which temperature influences mutation rate, and show that this single effect leads to dynamic temperature gradients in macroevolutionary rates and community structure. Early in community evolution, temperature strongly influences speciation and both speciation and extinction strongly influence species richness. Through time, niche structure evolves, speciation and extinction rates fall, and species richness becomes increasingly independent of temperature. However, significant temperature‐richness gradients may persist within emergent functional (trophic) groups, especially when niche breadths are wide. Thus, there is a strong signal of both history and ecological interactions on patterns of species richness across temperature gradients. More generally, the successful implementation of an eco‐evolutionary MTB opens the perspective that a process‐based MTB can continue to emerge through further development of metabolic models that are explicit in terms of functional traits and environmental gradients.     

Sex and destiny: The role of mating signals in speciation and macroevolution

A growing body of research posits a central role for mating signals in speciation and the reproductive isolation of species, yet there has been relatively little consideration of mating signal evolution within macroevolutionary theory. Factors that influence the divergence of fertilization systems generally, and mating signals specifically, may incidentally influence rates of speciation and patterns of species sorting. Potential key processes include: genetic drift, natural selection (differential survival), selection for mate recognition, and sexual selection. This paper explores the integration of mating signal evolution into macroevolution and hierarchy theory, arguing that speciational patterns may frequently result from “effect sorting”; in which microevolutionary processes operating at the organismal level have macroevolutionary effects at the clade level. Preliminary evidence indicates that sexual selection is a widespread and potent evolutionary force that, together with other mechanisms, may have a large, though incidental impact on species sorting. The Mate Competition Hypothesis is here proposed to account for this possibility, postulating that heritable, clade‐specific variations in the intensity of sexual selection and the potential breadth of signal‐receiver systems contribute to divergent patterns of species‐richness. Several examples from the vertebrate fossil record are consistent with this hypothesis.     

Is species selection dependent upon emergent characters?

The architects of punctuated equilibrium and species selection as well as more recent workers (Vrba) have narrowed the original formulation of species selection and made it dependent upon so-called emergent characters. One criticism of this narrow version is the dearth of emergent characters with a consequent diminution in the robustness of species selection as an important evolutionary process. We argue that monomorphic species characters may at times be the focus of selection and that under these circumstances selection at the organism level is by-passed due to the absence of critical variance. Selection therefore shifts to the species level where variability reemerges in a clade. The absence of critical variance among organisms prevents effect macroevolution from operating. If species-wide properties are important in macroevolutionary processes, as we contend, systematists should pay more attention to their elucidation.     

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.     

Biological hierarchies and the nature of extinction

Hierarchy theory recognises that ecological and evolutionary units occur in a nested and interconnected hierarchical system, with cascading effects occurring between hierarchical levels. Different biological disciplines have routinely come into conflict over the primacy of different forcing mechanisms behind evolutionary and ecological change. These disconnects arise partly from differences in perspective (with some researchers favouring ecological forcing mechanisms while others favour developmental/historical mechanisms), as well as differences in the temporal framework in which workers operate. In particular, long‐term palaeontological data often show that large‐scale (macro) patterns of evolution are predominantly dictated by shifts in the abiotic environment, while short‐term (micro) modern biological studies stress the importance of biotic interactions. We propose that thinking about ecological and evolutionary interactions in a hierarchical framework is a fruitful way to resolve these conflicts. Hierarchy theory suggests that changes occurring at lower hierarchical levels can have unexpected, complex effects at higher scales due to emergent interactions between simple systems. In this way, patterns occurring on short‐ and long‐term time scales are equally valid, as changes that are driven from lower levels will manifest in different forms at higher levels. We propose that the dual hierarchy framework fits well with our current understanding of evolutionary and ecological theory. Furthermore, we describe how this framework can be used to understand major extinction events better. Multi‐generational attritional loss of reproductive fitness (MALF) has recently been proposed as the primary mechanism behind extinction events, whereby extinction is explainable solely through processes that result in extirpation of populations through a shutdown of reproduction. While not necessarily explicit, the push to explain extinction through solely population‐level dynamics could be used to suggest that environmentally mediated patterns of extinction or slowed speciation across geological time are largely artefacts of poor preservation or a coarse temporal scale. We demonstrate how MALF fits into a hierarchical framework, showing that MALF can be a primary forcing mechanism at lower scales that still results in differential survivorship patterns at the species and clade level which vary depending upon the initial environmental forcing mechanism. Thus, even if MALF is the primary mechanism of extinction across all mass extinction events, the primary environmental cause of these events will still affect the system and result in differential responses. Therefore, patterns at both temporal scales are relevant.     

PATTERNS IN PHYLOGENETIC TREE BALANCE WITH VARIABLE AND EVOLVING SPECIATION RATES

Aspects of phylogenetic tree shape, and in particular tree balance, provide clues to the workings of the macroevolutionary process. I use a simulation approach to explore patterns in tree balance for several models of the evolutionary process under which speciation rates vary through the history of diversifying clades. I demonstrate that when speciation rates depend on an evolving trait of individuals, and are therefore “heritable” along evolutionary lineages, the resulting phylogenies become imbalanced. However, imbalance also results from some (but not all) models of “nonheritable” speciation rate variation. The degree of imbalance increases with the magnitude of speciation rate variation, and then for gradual evolution (but not punctuated equilibria) reaches an asymptote short of the theoretical maximum. Very high levels of rate variation are required to produce imbalance matching that found in real data (estimated phylogenies from the systematic literature). I discuss implications of the simulation results for our understanding of macroevolution.     

The ecological dynamics of clade diversification and community assembly

Clades diversify in an ecological context, but most macroevolutionary models do not directly encapsulate ecological mechanisms that influence speciation and extinction. A data set of 245 chordate, arthropod, mollusk, and magnoliophyte phylogenies had a majority of clades that showed rapid lineage accumulation early with a slowing more recently, whereas a small but significant minority showed accelerated lineage accumulation in their recent histories. Previous analyses have demonstrated that macroevolutionary birth-death models can replicate the pattern of slowing lineage accumulation only by a strong decrease in speciation rate with increasing species richness and extinction rate held extremely low or absent. In contrast, the metacommunity model presented here could generate the full range of patterns seen in the real phylogenies by simply manipulating the degree of ecological differentiation of new species at the time of speciation. Specifically, the metacommunity model predicts that clades showing decelerating lineage accumulation rates are those that have diversified by ecological modes of speciation, whereas clades showing accelerating lineage accumulation rates are those that have diversified primarily by modes of speciation that generate little or no ecological diversification. A number of testable predictions that integrate data from molecular systematics, community ecology, and biogeography are also discussed.     

Linking population‐level and microevolutionary processes to understand speciation dynamics at the macroevolutionary scale

Although speciation dynamics have been described for several taxonomic groups in distinct geographic regions, most macroevolutionary studies still lack a detailed mechanistic view on how or why speciation rates change. To help partially fill this gap, we suggest that the interaction between the time taken by a species to geographically expand and the time populations take to evolve reproductive isolation should be considered when we are trying to understand macroevolutionary patterns. We introduce a simple conceptual index to guide our discussion on how demographic and microevolutionary processes might produce speciation dynamics at macroevolutionary scales. Our framework is developed under different scenarios: when speciation is mediated by geographical or resource‐partitioning opportunities, and when diversity is limited or not. We also discuss how organismal intrinsic properties and different overall geographical settings can influence the tempo and mode of speciation. We argue that specific conditions observed at the microscale might produce a pulse in speciation rates even without a pulse in either climate or physical barriers. We also propose a hypothesis to reconcile the apparent inconsistency between speciation measured at the microscale and macroscale, and emphasize that diversification rates are better seen as an emergent property. We hope to bring the reader''s attention to interesting mechanisms to be further studied, to motivate the development of new theoretical models that connect microevolution and macroevolution, and to inspire new empirical and methodological approaches to more adequately investigate speciation dynamics either using neontological or paleontological data.     

Detecting the macroevolutionary signal of species interactions

Species interactions lie at the heart of many theories of macroevolution, from adaptive radiation to the Red Queen. Although some theories describe the imprint that interactions will have over long timescales, we are still missing a comprehensive understanding of the effects of interactions on macroevolution. Current research shows strong evidence for the impact of interactions on macroevolutionary patterns of trait evolution and diversification, yet many macroevolutionary studies have only a tenuous relationship to ecological studies of interactions over shorter timescales. We review current research in this area, highlighting approaches that explicitly model species interactions and connect them to broad‐scale macroevolutionary patterns. We also suggest that progress has been made by taking an integrative interdisciplinary look at individual clades. We focus on African cichlids as a case study of how this approach can be fruitful. Overall, although the evidence for species interactions shaping macroevolution is strong, further work using integrative and model‐based approaches is needed to spur progress towards understanding the complex dynamics that structure communities over time and space.     

Interactions within and between clades shaped the diversification of terrestrial carnivores

A longstanding debate in evolutionary biology and paleontology is whether ecological interactions such as competition impose diversity dependence on speciation and extinction rates. Here, we analyze the fossil record of terrestrial mammalian carnivores in North America and Eurasia using a Bayesian framework to assess whether their diversity dynamics were affected by diversity dependence within and between families (12 in Eurasia, 10 in North America). We found eight instances of within‐clade diversity dependence suppressing speciation rates and detected between‐clade effects increasing extinction rates in six instances. Diversity dependence often involved lineages that migrated between continents and we found that speciation was more responsive to diversity changes within the clade, whereas extinction responded to diversity of taxa in other clades. The analysis of the fossil record of Carnivora suggests that interactions within and between clades are associated with different speciation and extinction regimes, opening room for a broader theory of diversity dependence.     

Estimating diversification rates for higher taxa: BAMM can give problematic estimates of rates and rate shifts

Estimates of diversification rates are invaluable for many macroevolutionary studies. Recently, an approach called BAMM (Bayesian Analysis of Macro‐evolutionary Mixtures) has become widely used for estimating diversification rates and rate shifts. At the same time, several articles have concluded that estimates of net diversification rates from the method‐of‐moments (MS) estimators are inaccurate. Yet, no studies have compared the ability of these two methods to accurately estimate clade diversification rates. Here, we use simulations to compare their performance. We found that BAMM yielded relatively weak relationships between true and estimated diversification rates. This occurred because BAMM underestimated the number of rates shifts across each tree, and assigned high rates to small clades with low rates. Errors in both speciation and extinction rates contributed to these errors, showing that using BAMM to estimate only speciation rates is also problematic. In contrast, the MS estimators (particularly using stem group ages), yielded stronger relationships between true and estimated diversification rates, by roughly twofold. Furthermore, the MS approach remained relatively accurate when diversification rates were heterogeneous within clades, despite the widespread assumption that it requires constant rates within clades. Overall, we caution that BAMM may be problematic for estimating diversification rates and rate shifts.     

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.     

“And then a miracle occurs” — weak links in the chain of argument from punctuation to hierarchy

Weak links, in the form of inadequacies in both reasoning and supporting evidence, exist at several critical steps in the derivation of an hierarchical concept of evolution from punctuated equilibria. Punctuation itself is predicated on a distorted reading of phyletic change as phyletic gradualism, and of allopatric speciation as the instantaneous formation of unchanging typological taxa. The concept of punctuation is further confounded by the indescriminate employment of the same term to denote both a causal explanation for evolutionary change and an outcome of substantiated evolutionary processes. Even when the intended usage for the term is specified, each denotation of punctuation entails respective drawbacks. As a causal explanation, punctuation clearly belongs to the class of quantum theories with all their attendant impedimenta, including special salsatory non-adaptive mechanisms of evolutionary change. Redefinition of punctuation as a pattern of morphologic change reduces it to one possible outcome of known microevolutioanry processes, thus obviating any need for an hierarchical explanation of macroevolution. While vacillation between usages has preserved the term in the literature, the end result of this obfuscation has been a circle of faulty reasoning in which the pattern of punctuation is invoked as its own proof. Widespread confusion concerning what constitutes an adequate test of punctuation is directly attributable to imprecision in both the original and revised formulations of the concept.The argument for species-level selection is based on the typological and philosphically flawed premise of species as individuals, and further requires the hypothesis of heritable emergent properties, for which empirical evidence is lacking.Extrapolation of hierarchy to higher taxonomic levels depends on the unproven assumption that mass extinction constitutes a causal mechanism for macroevolution which is qualitatively distinct from, and not reducible to, the causes of microevolution.Because key elements of hierarchical theory depend upon misrepresentations of the synthetic theory, semantic circumvention, and questionable reasoning, and because its central assertions remain unsubstantiated by empirical evidence, the derivation of an hierarchical theory of evolution from punctuation constitutes an exercise an futility and should be abandoned.