What is Macroevolution? PDF

[Palaeontology, Vol. 63, Part 1, 2020, pp. 1–11] FRONTIERS IN PALAEONTOLOGY WHAT IS MACROEVOLUTION? by MICHAEL HAUTMANN Pal€aontologisches Institut und Museum, Universit€at Z€ urich, Karl-Schmid Strasse 4, 8006 Z€...

[Palaeontology, Vol. 63, Part 1, 2020, pp. 1–11] FRONTIERS IN PALAEONTOLOGY WHAT IS MACROEVOLUTION? by MICHAEL HAUTMANN Pal€aontologisches Institut und Museum, Universit€at Z€ urich, Karl-Schmid Strasse 4, 8006 Z€ urich, Switzerland; [email protected] Typescript received 14 June 2019; accepted in revised form 15 October 2019 Abstract: Definitions of macroevolution fall into three cat- intraspecific competition as a mediator between selective egories: (1) evolution of taxa of supraspecific rank; (2) evolu- agents and evolutionary responses. This mediating role of tion on the grand time-scale; and (3) evolution that is guided intraspecific competition occurs in the presence of sexual by sorting of interspecific variation (as opposed to sorting of reproduction and has therefore no analogue at the macroevo- intraspecific variation in microevolution). Here, it is argued lutionary level where species are the evolutionary units. Com- that only definition 3 allows for a consistent separation of petition between species manifests both on the macroevolution and microevolution. Using this definition, spe- microevolutionary and macroevolutionary level, but with dif- ciation has both microevolutionary and macroevolutionary ferent effects. In microevolution, interspecific competition aspects: the process of morphological transformation is spurs evolutionary divergence, whereas it is a potential driver microevolutionary, but the variation among species that it pro- of extinction at the macroevolutionary level. Recasting the Red duces is macroevolutionary, as is the rate at which speciation Queen hypothesis in a macroevolutionary framework suggests occurs. Selective agents may have differential effects on that the effects of interspecific competition result in a positive intraspecific and interspecific variation, with three possible sit- correlation between origination and extinction rates, confirm- uations: effect at one level only, effect at both levels with the ing empirical observations herein referred to as Stanley’s rule. same polarity but potentially different intensity, and effects that oppose between levels. Whereas the impact of all selective Key words: macroevolution, definition, species selection, agents is direct in macroevolution, microevolution requires competition, Red Queen hypothesis, extinction rates. E V O L U T I O N can be studied from two decidedly different in this discussion is the role of competition, which demon- perspectives: the study of the processes that lead to evolu- strates that evolutionary processes do not always operate tionary change and reproductive isolation within and analogously in microevolution and macroevolution. among populations, and the study of the long-term fate of species or higher-rank taxa through geologic time. These two perspectives correspond broadly to two different disci- DEFINITIONS plines (biology and palaeontology) and are usually referred to as microevolution and macroevolution. Yet, does this distinction indicate two operationally different levels of ‘It would be useful to define “macroevolution”, but evolution or merely a difference between disciplines or definitions vary.’(Futuyma 2015, p. 30) scales? Different opinions about this question are reflected by different definitions of macroevolution, and conversely, different definitions imply different answers to it. In this context, the purpose of this paper is twofold. First, it Definition 1: Macroevolution as the evolution of taxa of explores existing definitions of macroevolution and asks supraspecific rank how the choice of definition affects the categorization of evolutionary processes as either microevolutionary or The term ‘macroevolution’ was introduced by Phi- macroevolutionary. Second, implications of a strictly con- liptschenko (1927, p. 93), who referred it to the evolution ceptual definition of macroevolution are discussed with of taxa above the species level in the Linnaean hierarchy respect to the differential effect of selective agents at the (genera, families, orders, etc.) His motivation for distin- microevolutionary versus macroevolutionary level. A focus guishing the evolution of higher-rank taxa from © The Palaeontological Association doi: 10.1111/pala.12465 1 2 PALAEONTOLOGY, VOLUME 63 ‘micro’evolution was the belief that major body plan modi- discussed below. Levinton’s (2001, 2012) definition of fications cannot arise through the summation of the small- macroevolution as ‘the sum of those processes that explain scale changes on which Darwinian evolution is based. This the character state transitions that diagnose evolutionary dif- view was very common at his time, and Philiptschenko’s ferences of major taxonomic rank’ escaped from such ambi- (1927) book is mainly a review of existing work on the guity, but the problem of a clear distinction between topic, with the purpose of setting an agenda for future microevolution and macroevolution under this definition research. Theoretical underpinning followed. Goldschmidt persists. As Levinton (2001, p. 2) wrote: ‘It is not useful to (1933) suggested that mutations that affect the rates of distinguish sharply between microevolution and macroevolu- developmental processes could lead to sudden, saltational tion’. This statement is true in the context of his above-cited changes in the phenotype that are mostly detrimental, but definition of macroevolution, but it is also an admission of in rare cases will produce ‘hopeful monsters, monsters its inadequateness. which would start a new evolutionary line if fitting into some empty environmental niche’ (Goldschmidt 1933, p. 547). Later, Goldschmidt (1940) added to this developmen- Definition 2: Macroevolution as a phenomenological term tal argument his idea of alterations in the chromosomal for evolution on the grand time-scale pattern as an explanatory mechanism for the postulated hopeful monsters, which catalysed partly polemic criticism When Dobzhansky (1937, p. 12) introduced the term of his concept in general (see Gould 2002, pp. 451–466 and ‘macroevolution’ to the English-speaking community, he Rieppel 2017, pp. 109–125 for detailed discussions). The added a time-perspective to the concept in saying that modern assessment is more conciliatory and acknowledges ‘macro-evolutionary changes... require time on a geologi- some possible examples of hopeful monsters, mostly cal scale’. After the rejection of the concept of macroevolu- involving mutations of genes that regulate key developmen- tion propagated by Goldschmidt (1940) and others, time- tal processes during ontogeny (e.g. Chouard 2010; Page scale became an alternative basis for the definition of the et al. 2010; Rieppel 2017). This explanatory scenario is term. For example, Dawkins (1982, p. 289) defined reminiscent of Goldschmidt’s (1933) original concept and macroevolution as ‘the study of evolutionary changes that led some researchers to the conclusion that evolutionary take place over a very large time-scale’ and added that the developmental biology (evo-devo) ‘clearly paved the way term should be used as a ‘neutral label’ unburdened by the- for a revival of saltational evolution’ (Theißen 2009, p. 46). ory. Grantham (1995, p. 302) was more precise with regard (This potential for saltational evolution must be distin- to ‘time-scale’ by defining macroevolution ‘to be the guished from a possible macroevolutionary role of develop- domain of evolutionary phenomena that require time mental processes in biasing the production of variation, spans long enough to be studied using paleontological which is discussed below.) In spite of such rehabilitations, a techniques’. These time-scale based definitions allow the definition of macroevolution as the saltational origin of incorporation of all processes that affect the long-term pat- new body plans caused by developmental genetic changes terns of evolution, from biotic interactions to global envi- remains problematic. The reason is not so much that this ronmental changes. This inclusiveness is the reason for process is theoretically impossible, but rather that develop- their attractiveness as consensus definitions but, similar to mental processes do not establish a qualitative break definition 1, they do not provide clear-cut criteria for cate- between two levels of evolutionary change (e.g. Arthur gorizing a given process as either microevolutionary or 2003; Hoekstra & Coyne 2007; Nunes et al. 2013; Futuyma macroevolutionary. The vagueness in this respect results 2015) that would allow for a consistent separation between from the trivial fact that virtually all evolutionary processes, microevolution and macroevolution. regardless of their magnitude, can at least theoretically In spite of the failure to identify a qualitative difference sum-up over geologic time to gain relevance on the grand between the underlying processes, the distinction between time-scale. Distinguishing macroevolution from microevo- microevolution and macroevolution based on the level of lution by the scale of observation is therefore a convenient taxonomic observation persisted. The most common formu- practice for designating different scopes within evolution- lation that is still used today is that of macroevolution as ary research, but it remains diffuse as a definition and pro- ‘evolution above the species level’, which was probably popu- vides no basis for conceptual advances in the field. larized by the title of Rensch’s (1959) book. Originally refer- ring solely to the evolution of characters that distinguish taxa above the species level, it is often referred today to patterns Definition 3: Macroevolution as evolution that is guided by and causes of diversification of higher taxa, such as variation sorting of interspecific variation in diversity, speciation rates, and extinction among clades (Futuyma 2015, p. 30). If used in the latter sense, ‘evolution The idea that species are units of selection dates back to above the species level’ includes aspects of definitions 2 and 3 de Vries (1905) and has reappeared independently several  HAUTMANN: MACROEVOLUTION 3 times since then (see Gould 2002). However, it is fair to of supraspecific rank) but extinction is not, because say that Stanley (1975) was the first to formulate a testa- extinction does not contribute to the evolution of new ble hypothesis on ‘species selection’ and to expound its morphologies. Under definition 3, extinction is a central consequences for the hierarchical structure of evolution. macroevolutionary process (analogous to death in Accordingly, speciation decouples macroevolution from microevolution; Stanley 1975), whereas speciation has microevolution, and macroevolution is guided through both a microevolutionary and a macroevolutionary differences in speciation and extinction rates. Subsequent aspect. The process of morphological transformation research (e.g. Vrba & Gould 1986; Jablonski 2008a; and between species is always microevolutionary (contrary to refs therein) distinguished between ‘strict sense species definition 1), because it occurs through selection among selection’, where selection occurs on traits that are emer- intraspecific variation. This also applies to punctuated gent at the species level (e.g. geographical range), from equilibrium, which is sometimes seen incorrectly as a ‘effect macroevolution’, which occurs by selection on macroevolutionary model of speciation (e.g. Hoekstra & aggregate organismic traits (Stanley’s original concept). If Coyne 2007). In contrast, the outcome of speciation as the focal level of selection is not specified, ‘species sort- the source of interspecific variation is macroevolutionary, ing’ has conventionally been used as a neutral term that analogous to mutation and recombination as the source avoids a statement about the causes for the differential of variation in microevolution (Stanley 1975). success among species. Later, Lloyd & Gould (1993) and It should be noted that Stanley (1975, 1979) did not Gould (2002, pp. 656–673) regarded the ‘strict sense spe- use species selection explicitly for defining macroevolu- cies selection’ concept (= ‘emergent character concept’ in tion. Rather, he introduced his concept as ‘a theory of their new terminology) as too restrictive. Instead, they evolution above the species level’ (Stanley 1975) and thus argued that any pattern of differential speciation and as an explanatory model for macroevolutionary phenom- extinction rates that correlates with a trait emergent at ena in the sense of existing definitions. Notably, Stanley’s any hierarchical level is a case of species selection (1979) textbook on macroevolution avoids a definition of (‘emergent fitness concept’; see Lieberman & Vrba 2005 the field, and species selection plays a surprisingly subor- for further discussion). An important argument in favour dinate role in this work, although Stanley (1979, pp. ix– of the ‘emergent fitness concept’ is that species selection x) emphasized that ‘the species is the natural (if imper- acting on aggregate organismic traits can theoretically fect) unit of macroevolution’. Later, Gould (1980) linked oppose selection at the organismic level and is therefore macroevolution indirectly with species selection by defin- not reducible to this level (Grantham 1995). In this ing it as the differential success among species, which is paper, I use ‘species selection’ in its broad sense based on the obvious outcome of species selection (or sorting) and the emergent fitness concept and refer to ‘species sorting’ thus at least an implicit reference to that concept. I there- when the term ‘selection’ appears inappropriate; e.g. in fore regard species sorting as the essence of a third cate- order to include cases of species drift or cases where the gory among the existing definitions of macroevolution, trait under selection is not heritable. although to my knowledge this has not yet been proposed Stanley’s (1975) paper stimulated a vigorous discussion explicitly. and plenty of subsequent research (see summaries in: Gould 2002; Jablonski 2008a, 2017a) but remarkably, it remained largely unnoticed that a substantial change in Choice of definition the scope of macroevolution was implicit in the new con- cept. Macroevolution according to the new concept no Currently, the neutral definition of macroevolution as longer referred to the processes of morphological change evolution on the grand time-scale (definition 2) is most that lead to evolutionarily new taxa of supraspecific rank widely used, but this definition does not provide criteria (definition 1), but instead to the differential evolutionary for a consistent distinction between microevolutionary success of clades through geologic time, caused by differ- and macroevolutionary processes, which renders it con- ences in speciation and extinction rates (Gould 1980, ceptually useless. Referring macroevolution to the evolu- 1985). This change in scope is exemplified, among other tion of taxa of supraspecific rank (definition 1) has the things, by the different roles that speciation and extinc- advantage that it is in accordance with the original scope tion have in definitions 1 and 3. Most workers intuitively of macroevolution. However, it is undisputed today that regard both speciation and extinction as macroevolution- all evolutionary change involves intraspecific modifica- ary (including those who follow definition 1; e.g. Levin- tion, regardless of the quantity of the change, and that in ton 2001) but this practice is not in accordance with a this sense macroevolution would be indeed reducible to strict interpretation of the different definitions. Under microevolution (e.g. Erwin 2000). Definition 3 is concep- definition 1, speciation is potentially macroevolutionary tually different from the original definition, but it allows (if it leads to species that establish evolutionarily new taxa the unequivocal distinction between microevolution 4 PALAEONTOLOGY, VOLUME 63 (where organisms are the units of sorting) and macroevo- Jablonski 2008a). Predation, for example, may cause lution (with species as units of sorting). Given the funda- microevolutionary changes within a prey species by placing mental difference to the original definition, it would be individuals with certain antipredatory features at a selective desirable to introduce a new term for evolution that is advantage (situation 1 in Fig. 1A), or cause species selec- guided by species sorting, but it is unlikely that a new tion by driving one prey species to extinction and another nomenclature would find broad acceptance. I therefore not (situation 2 in Fig. 1A), or have variable effects at both suggest retaining the term macroevolution for evolution levels (Fig. 1B; see below for further explanations). More- in the sense of definition 3, based on the concept of Stan- over, selection for a trait at one level can oppose selection ley (1975) and others, and abandoning definitions 1 and for the same trait at another level (Grantham 1995; Jablon- 2. Because selection requires variation, I suggest the fol- ski 2008a). This section discusses the basic principles that lowing formulation: Macroevolution is evolutionary change underlie the differential impact of selective agents at the that is guided by sorting of interspecific variation. microevolutionary and macroevolutionary levels. The answer to the question of whether selection occurs at the microevolutionary or macroevolutionary level is triv- Generation of variation: microevolutionary versus ial in the case of ‘strict sense species selection’ (see Jablon- macroevolutionary aspects ski 2008a for a comprehensive overview), where the trait under selection resides exclusively at the level of the species, Classic population-genetic models of microevolution or, but not on the organismic level (e.g. sex ratio or geographi- more generally, natural selection as originally formulated cal range). In such cases, selection occurs evidently only by Darwin (1859), are based on the premise that among interspecific variation; i.e. macroevolution. intraspecific variation is ‘random’ in the sense that it is The problem becomes more complicated if selection unrelated to the direction of evolutionary change (e.g. acts on traits that are variable between different organ- Gould 2002, p. 144). Stanley (1975) made a similar case isms of a population and between different co-existing for macroevolution by suggesting that speciation as the species, a situation that applies to most morphological, source of interspecific variation is random as well. These physiological or behavioural traits. A key requirement for premises have been challenged by the recognition that a macroevolutionary effect of selection in this situation is developmental systems can impose a bias on the pheno- that the trait under selection exhibits little or no variation typic variation on which selection operates at any level within species relative to the variation among species (e.g. Gerber 2014; Wagner 2014; Uller et al. 2018). (Jablonski 2008a). There is currently no consensus about whether the Figure 1A–B illustrates how intra versus interspecific impact of developmental systems on the non-random variation and the focus of selection with respect to these generation of variation can be accommodated within variations combine to either a microevolutionary or a microevolution (e.g. Futuyma 2015) or constitute a dif- macroevolutionary response. The common theme in both ferent case that falls within the field of macroevolution examples is that the focus of selection relative to the trait (e.g. Erwin 2017; Jablonski 2017b; Uller et al. 2018). In variation determines whether selection occurs within or the context of the definition of macroevolution advo- between species. cated herein, as sorting of interspecific variation, biased In the first example (Fig. 1A), it is assumed that a preda- production of interspecific variation can be seen as an tor appears in an ecosystem that contains two potential analogue of sorting (corresponding to Erwin’s (2017) prey species A and B, and that the sole antipredatory strat- ‘developmental push’) that precedes species sorting by egy of these two species is escape. Equivalents of this sim- distributional processes, and might therefore be accom- plified hypothetical case are invasive predatory species in modated within macroevolution. present-day ecosystems (see Short et al. 2002 for some examples) or major evolutionary improvements of preda- tory skills in the geological past. In the illustrated case AGENTS OF SELECTION: (Fig. 1A), the two different hunting speeds 1 and 2 of the MICROEVOLUTIONARY VERSUS predator with respect to intraspecific versus interspecific MACROEVOLUTIONARY EFFECTS variation of the maximum escape speed of the potential prey species determine whether the effect of the predator Distinguishing microevolution and macroevolution by the on the prey is microevolutionary or macroevolutionary. level of sorting (organisms vs species) not only allows for a Hunting speed 1 introduces a selection pressure favouring clear conceptual separation, it also puts emphasis on an adaptations for faster running in the population of prey aspect of evolution that is often ignored: the causes of evo- species A, because the hunting speed is within the range of lution can only be understood if the effects of selective the escape speed of some individuals of this species and agents are analysed for both levels (e.g. Gould 2002; these faster running individuals are at a selective advantage  HAUTMANN: MACROEVOLUTION 5 FIG. 1. Microevolutionary versus macroevolutionary effects of selec- tive agents. A, hypothetical case of a predator that appears in an ecosys- tem with two prey species; hunting speed 1 allows for a microevolution- ary response of prey species A, whereas hunting speed 2 poses prey species B at a selective advantage over prey species A, which cannot respond by microevolutionary change; selection will therefore occur among interspecific variation (i.e. macroevolutionary) and poten- tially drive species A to extinction. B, overlapping variation of two spe- cies with respect to a relevant trait results in a fluent transition between three situations, depending on the focus of selection: (1) microevolu- tionary responses of both species (yellow, centre); (2) macroevolu- tionary response (green); and (3) macroevolutionary response plus microevolutionary response of the favoured species (orange); note that the fluent transition between the effects does not imply a transitions between the levels. See text for fur- ther details. over slower individuals in the population. Hunting speed 1 within two species overlap with respect to a selectively therefore allows for a microevolutionary response of prey relevant trait. Depending on the focus of selection, this species A to the appearance of the predator; prey species B situation results in a gradual transition between will remain unaffected because all of its individuals can microevolutionary responses of both species (Fig. 1B, yel- escape easily from attacks of the predator. Prey species B low area) and species selection that potentially eliminates will remain unaffected by the appearance of a predator with one of them (Fig. 1B, green areas). If extreme trait values the higher hunting speed 2 as well, but in this case, species are selected for, a microevolutionary response of the A cannot respond by microevolutionary change, because favoured species will occur in addition to the macroevo- this hunting speed is far beyond the escape speed of its fast- lutionary effect (Fig. 1B, orange). The crucial point in est individuals. In other words, species A lacks organisms this example for understanding the rationale behind the that have a relevant selective advantage within the popula- micro/macroevolution divide is that the gradual transition tion and this prevents a microevolutionary response. Intro- between the effects on the microevolutionary and duction of predator 2 will therefore lead to selection among macroevolutionary level does not constitute a transition the interspecific variation with respect to maximum escape between these levels themselves. Rather, the relative effect speed of the two potential prey species and may drive prey of the selection pressure on either of these levels changes species A to extinction; this is a macroevolutionary case. in response to its focus, whereas microevolution and Gould (2002, p. 665) characterized this situation more gen- macroevolution continue to operate independently. erally: ‘The species doesn’t die because organism A, B, or C, possesses a trait that had become maladaptive; the species dies because none of its parts (organisms) can develop any COMPETITION IN MICROEVOLUTION other form of the trait – and this lack of variation charac- AND MACROEVOLUTION terizes the species, not any of its individuals.’ Distinction between microevolutionary and macroevo- Competition occurs between individuals of the same species lutionary effects is not always as clear-cut as in this exam- (intraspecific competition) as well as between individuals of ple. Figure 1B illustrates a case in which the variation different species (interspecific competition). An obvious and 6 PALAEONTOLOGY, VOLUME 63 operationally relevant difference between microevolution promotion of niche differentiation and thus speciation and macroevolution with respect to competition is that (e.g. Mayr 1963; Schluter 1994; Emerson & Kolm 2005; organisms (the microevolutionary case) can be subject to Meyer & Kassen 2007; Pfennig & Pfennig 2012; Bailey both intraspecific and interspecific competition, whereas et al. 2013; Calcagno et al. 2017). In this microevolution- species as evolutionary individuals (the macroevolutionary ary role, interspecific competition is the ‘centrifugal force case) can only be subject to interspecific competition. of evolution’ (Mayr 1963), but it also contributes to the generation of interspecific variation that is subject to selection at the macroevolutionary level (Fig. 2). The pre- Intraspecific competition: mediator of selective agents in requisite for a microevolutionary effect of interspecific microevolution competition is that variation of the trait under selection overlaps between competing species, as illustrated in Fig- Darwin (1859) addressed both intraspecific and interspeci- ure 1B. fic competition without making an explicit operational dif- In macroevolution, the outcome of interspecific com- ference between them, except from his repeated statements petition is essentially binary, either causing displacement that competition is most severe between individuals of the or extinction of the ill-adapted species, or permitting same species (e.g. Darwin 1859, p. 75). However, a privi- coexistence. In this aspect, interspecific competition does leged role of intraspecific competition is implicit in his the- not differ from other selective agents in macroevolution. ory of natural selection, which in essence holds that It should be noted, however, that the displacement/ex- intraspecific competition mediates between selective agents tinction alternative has opposing effects on biodiversity: and evolutionary change through its effects on the repre- extinction obviously causes a decrease in species richness, sentation of offspring in the next generation. Without whereas geographical displacement may increase richness intraspecific competition, there would be no microevolu- at the level of beta-diversity (Hautmann 2014). Interspeci- tionary response to any kind of selective pressures, includ- fic competition might also affect rates of speciation, either ing interspecific competition. This profound difference in negatively, by depressing population sizes of isolates and the microevolutionary role of intraspecific and interspecific thus their probability of surviving to speciation, of posi- competition stands in contrast to the effects of competition tively, by causing local extinctions and so promoting allo- on individual fitness, where it is irrelevant whether a con- patric speciation (Jablonski 2008b, p. 723). specific or heterospecific competitor detracts from the Summarized (Table 1), competition in microevolution resources of an organism. occurs: (1) as intraspecific competition, which has a cen- Although intraspecific competition alone may promote tral and unique role at this level in mediating between speciation (e.g. Svanb€ack & Bolnick 2007; Pfennig & Pfennig selective agents and evolutionary response; and (2) as 2012), its momentum as a driver of evolutionary divergence interspecific competition, which is a main driver of evolu- is weak if it does not mediate external selective agents such as tionary divergence. In contrast, competition in macroevo- interspecific competition. This situation is exemplified in the lution manifests solely between species and affects co- aftermath of the end-Permian mass extinction, where diversi- existing species either directly by replacement, or it fication rates of many taxa remained extremely low for several remains macroevolutionarily neutral (which, of course, million years because so many competing species had become does not exclude a potential microevolutionary effect). extinct (Hautmann et al. 2015; Pietsch et al. 2018). Examples What is the ultimate cause of these differences in the role of intraspecific competition developing its own evolutionary of competition in microevolution and macroevolution? dynamic do occur (Pfennig & Pfennig 2012) but if this inter- nal dynamic is completely unrelated to the external environ- ment (biotic or abiotic) its results might be negative at the Intraspecific versus interspecific competition in microevolution macroevolutionary level. Cases in which increased organismic and macroevolution fitness increases species’ vulnerability to extinction have been made in the context of sexual selection (e.g. McLain et al. To answer this question, it is helpful to compare the role 1999; Moen et al. 1999; Martins et al. 2018), which is obvi- of intraspecific competition for change at the microevolu- ously unrelated to any external agents of selection. tionary level with that of interspecific competition at the macroevolutionary level. Let us consider the differential responses to an environmental factor (e.g. climatic cool- Interspecific competition: disentangling microevolutionary ing) at these two levels. In the microevolutionary case, and macroevolutionary effects individuals with thicker fur within a population of a mammal species might have a selective advantage when In contrast to intraspecific competition, the principal temperatures decline and enrich their genes in the gene effect of interspecific competition in microevolution is pool relative to competitors with a less thick fur, which  HAUTMANN: MACROEVOLUTION 7 FIG. 2. Summary chart illustrating how microevolution and macroevolution combine to produce biodiversity and evolutionary change. Colour online. leads to evolutionary change. Here, intraspecific competi- TABLE 1. Roles of intraspecific and interspecific competition tion mediated between selective agent and evolutionary in microevolution and macroevolution. response. On the macroevolutionary level, cooling might Microevolution Macroevolution similarly help a mammal species with thick fur to out- compete a species with less thick fur, apparently analo- Intraspecific Mediates all other — gously to the microevolutionary case. In contrast to competition agents of selection; microevolution, however, a mediating role of competition weak driver of is not necessarily involved in macroevolutionary change. evolutionary change without this Cooling can increase the number of species with thick fur mediating role within a clade even in complete absence of interspecific Interspecific Major driver of Underlies positive competition, solely by driving less well-adapted species to competition morphological correlation between extinction. The reason for this microevolutionary differ- divergence speciation and ence lies in the fact that sexual reproduction has no extinction rates equivalent in macroevolution, which constitutes a princi- pal difference in how evolution works at these two levels. In microevolution, the units of selection (organisms) are allied by gene pools and gene flow, whereas species in a a gene pool) and is therefore not inherently negative for clade are inert entities that only share common ancestry the success of other species within the clade, unless these (cases of hybridization or lateral gene transfer might rep- are direct competitors (see below). This case highlights resent a third, somehow intermediate situation that is not the fact that evolutionary processes in microevolution treated herein). Accordingly, macroevolutionary success and macroevolution are not completely analogous, and of a species with an advantageous trait is not laterally demonstrates that a clear conceptual definition of the transferred within its clade (in absence of an analogue of fields facilitates the recognition of such differences. 8 PALAEONTOLOGY, VOLUME 63 Interspecific competition in macroevolution: data and 1973, figs 1–7), which are the empirical basis for the ‘law theoretical conclusions of extinction’, are reflections of stasis rather than of perma- nent change within taxa, because the extended existence Although interspecific competition as a selective agent time of fossil taxa implies constant morphologies. (Mor- operates in macroevolution in the same way as any other phology is the basis for the identification of fossil taxa, and selective agents by directly affecting (or not affecting) the an extended time of existence of a taxon can only be existences of species, its macroevolutionary role might be inferred if its morphology remains stable over this time.) more pervasive than that of most other factors. This con- Thus, ironically, the empirical basis of the RQH hypothesis clusion is indicated by the observation that origination holds only under the evolutionary regime of punctuated and extinction rates are usually positively correlated in a equilibria (PE), where morphological change is concen- given clade. Recently, Marshall (2017) called this empiri- trated in speciation events (Eldredge & Gould 1972). cal rule ‘the third law of palaeobiology’ but I suggest the Fortunately, recasting the RQH in the framework of PE term ‘Stanley’s rule’ in recognition of the work of Steven is conceptually unproblematic, because it is irrelevant in Stanley, who was the first to address this phenomenon in the RQH whether the evolutionary increase in fitness detail (Stanley 1979, 1985, 1990). Stanley’s rule is proba- occurs continuously or during speciation events. In a PE bly the most general macroevolutionary rule; it is there- context, the RQH simply implies that each speciation fore surprising that it found relatively little interest in the event in a clade deteriorates the fitness of coexisting spe- subsequent literature. Stanley (1990) attributed the posi- cies, which predicts a positive correlation between the tive correlation between origination and extinction rates rates of speciation and extinction in this clade (i.e. Stan- to five ecological factors: behavioural complexity, niche ley’s rule). Eventually, this argument from the RQH goes breadth, population size and stability, dispersal ability back to Darwin’s (1859) notion that closely related spe- and habitat fragmentation. Each of these factors is cer- cies compete most intensely, or, more generally, that tainly relevant, but I suggest here that Stanley’s rule is members of a clade are on average stronger competitors primarily a macroevolutionary aspect of van Valen’s than phylogenetically more distant species (niche conser- (1973) Red Queen hypothesis (RQH). vatism; see Pyron et al. 2015 for a recent review). Van Valen (1973) derived his RQH from two observa- Research interest in the RQH has revived in recent years, tions: (1) the probability of extinction of a taxon is con- with a lively debate between critics (e.g. Finnegan et al. stant and independent of its age (the ‘law of extinction’); 2008; Vermeij & Roopnarine 2013) and supporters (e.g. (2) the probability of extinction is strongly related to  Quental & Marshall 2013; Zliobait_ e et al. 2017). The adaptive zones, because different taxa have different prob- match of RQH predictions with Stanley’s rule adds an abilities of extinction. In other words, extinction occurs argument in support of the RQH to this debate. randomly with respect to age but nonrandomly with It should be noted that Stanley (1979, p. 229, 270) respect to ecology. Collectively, these two observations rejected the possibility that the correlation between origi- suggest that the effective environment of any homoge- nation and extinction rates results from niche crowding, neous group of organisms deteriorates at a stochastically which enables speciation only after extinction has made constant rate. Van Valen (1973) proposed that this is the niche space available. His reservation against a niche result of an evolutionary zero-sum game driven by inter- crowding explanation stems from the fact that his data specific competition: the evolutionary progress (= increase for rates of diversity increase (a surrogate for speciation in fitness) of one species deteriorates the fitness of coex- in that work) in the discussed taxa were taken from geo- isting species, but because coexisting species evolve as logic times of rapid diversification, where availability of well, no one species gains a long-term increase in fitness, niche space was apparently not a limiting factor. and the overall fitness of the system remains constant. Although cause-and-effect is opposite in the niche crowd- The name of the RQH refers to Lewis Carroll’s book ing explanation (where extinction makes room for specia- Through the Looking-Glass, in which the Red Queen (a rep- tion) and in the Red Queen explanation (where resentation of a chess piece) says: ‘It takes all the running speciation is a cause of extinction), the underlying control you can do, to keep in the same place.’ The metaphorical in both models is interspecific competition, which either name implies permanently ongoing change, which was prevents speciation or causes extinction. Does this mean probably intended by van Valen (1973), but this connota- that Stanley’s (1979) argument also casts doubt on the tion is unfortunate. As Vermeij & Roopnarine (2013, p. Red Queen explanation advocated herein? I think that 563) stated, the RQH provides a microevolutionary expla- there is a relevant difference, which results from the nation (continuous adaptive evolution within species) for a reversed cause-and-effect relationship of speciation and macroevolutionary phenomenon (constant extinction risk extinction in the two explanations. Stanley’s (1979) argu- of taxa within a clade). Going one step further, it can be ment holds for questioning a niche crowding explanation, argued that the taxonomic survivorship curves (van Valen but in a Red Queen explanation where speciation causes  HAUTMANN: MACROEVOLUTION 9 extinction, niche conservatism becomes an additional and Macroevolution as understood herein does not produce critical factor. Niche space might have been largely empty evolutionary novelties, but it determines their proliferation during the episodes of rapid diversification that Stanley within the clades in which they evolved, and it adds species- (1979) analysed, but if daughter species are as a rule eco- level traits as non-organismic factors of sorting to this pro- logically very similar to their parent species, then compe- cess. In this way, macroevolution eventually determines the tition between them remains a relevant factor even if fate of microevolutionary change. more distant niche space is still unoccupied. A second note concerns the question of how the intensity Acknowledgements. I thank Jonathan Payne (Stanford) for his of interspecific competition affects the correlation between helpful comments on this manuscript. Constructive reviews by speciation and extinction. It might be predicted alterna- D. 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