Focused Essay
Hypotheses of adaptive evolution: Escalation and the Red Queen
Submitted by Haley Glass
To the Department of Biological Sciences
at the University of Calgary
in partial fulfillment of the requirements
for the degree of Doctor of Philosophy
PhD Candidacy Examination
December 5, 2017
Question
Describe (i) evolutionary escalation (Vermeij, 1987, Evolution & Escalation: An
Ecological History of Life, Princeton University Press) and (ii) the Red Queen
Hypothesis (Van Valen, 1973, Evolutionary Theory, 1: 1–30). In doing so, discuss
how they differ from each other.
Abstract
Introduction
Coevolution: Cott 1940
Biological diversity is highly dynamic, with species and entire lineages rising and falling over
time. The dynamics of diversification are determined by the balance between speciation and
extinction rates, which may vary in response to catastrophic events (Alvarez et al. 1980; Renne et al.
1995), changing environments (Alroy et al. 2000; Fortelius et al. 2006; Ezard et al. 2011), and biotic
interactions (Jablonski and Sepkoski 1996; Liow et al. 2015; Silvestro et al. 2015). Although major
macroevolutionary phenomena such as mass extinctions seem to be largely driven by abiotic factors
(Benton 2009), ecological interactions most certainly played a significant role in shaping the
diversification of several lineages (Voje et al. 2015).
The aim of this paper is to (i) elucidate the conceptual differences between the hypothesis of escalation and the Red Queen Hypothesis, (ii) clarify their views on selection pressures, coevolutionary arms races, and evolutionary time scales are clarified, and (iii) describe applications of these theories to examples of enemy-victim interactions.
Hypotheses of adaptive evolution
Red Queen Hypothesis
In "A new evolutionary law" Van Valen (1973) generated a hypothesis to describe his idea that taxa experience constant rates of extinction within an effective environment, also referred to as an adaptive zone (Van Valen 1971). He first suggests the Law of Extinction, the theory that for a group of organisms, the biotic environment deteriorates at an approximately uniform rate, and therefore the probability of extinction is independent of a given taxon's age. Motivated by examples in the paleontological record, Van Valen (1973) finds that over 25,000 subtaxa display almost uniform linearity of extinction rates. For each taxa (e.g. Brachiopoda, Mammalia, Reptilia), the log number of subtaxa surviving versus their durations was plotted, yielding linear survivorship curves (Figure 1). He then argues that few exceptions to this trend are seen in the fossil record.
Figure 1. Example of a linear extinction rate of a taxon, displayed by plotting log number of subtaxa versus their duration in millions of years. Data is random and generated only to display the general trend. Adapted from Liow et al. 2011, page 350.
Seeking to explain the Law of Extinction, Van Valen (1973) developed the Red Queen hypothesis. The name of the hypothesis is inspired by the famous line from Lewis Carroll's Through the Looking Glass (1871) when the Red Queen says to Alice, "Now here, you see, it takes all the running you can do to keep in the same place." The Red Queen reflects the idea that species must always be evolving, or running in place, in order to keep up with the constantly deteriorating biotic environment. According to this hypothesis, the observed extinction rates in the fossil record can be attributed to the evolution of competing species within the environment. The RQH assumes that adaptation by one species has an equal and opposite effect on all other species within its effective environment, and that extinction and adaptation are closely tied processes. Essentially, when one species experiences an increase in fitness, this equates to a total decline in fitness for the other species within its adaptive zone. The hypothesized stochasticity throughout evolutionary time also suggests a long-term constancy in the rate of molecular evolution (Van Valen 1974).
While originally proposed as an answer to the Law of Extinction, the RQH has come to be one of the most well known theories of enemy-victim coevolution (refs). Because the RQH focuses on a deteriorating biotic environment, this does not include abiotic factors and therefore places the emphasis on interactions between competitive or antagonistic species interactions, unifying all trophic levels within the framework (Brockhurst et al. 2014, Liow et al. 2011). The coevolution of competing species may eventually lead to extinction unless they are able to adapt and counteract the changes experienced within their biotic environment. However, their relative fitness remains unchanged, suggesting that evolution is a zero-sum game (Van Valen 1973). The idea of coevolution under the Red Queen has been applied to predator-prey interactions, where in order to keep up with their evolving predators, prey species must constantly evolve to survive, so they exhibit reciprocal selection on one another. In addition, other interpretations of the RQH have suggested an advantage of sexual versus asexual reproduction in individuals, specifically in regards to host-parasite interactions (i.e. Lively 2000, Lively 2010).
Overall, the Red Queen Hypothesis is suggested as a microevolutionary explanation of the macroevolutionary observation of constant extinction. On the species-level, the RQH implies that constant changes within the biotic environment are due to competitive interactions between enemies and victims. The changes in species are subsequently responsible for the macroevolutionary trend of adaptive evolution and the extinction rates seen within the fossil record. The closely tied interactions between enemy and victim highlighted by the RQH may also lead to a coevolutionary arms race (Dawkins & Krebs 1979, Dawkins 1986). In response to changes in an enemy species, the victim must continually increase their defenses in response to selection pressure by the enemy, who then reciprocally evolves to counteract the change (Futuyma & Slatkin 1983). This constant cycle of reciprocal coevolution under the RQH has come to be known as Red Queen dynamics (Marrow et al. 1992).
Hypothesis of Escalation
The theory was first proposed to explain the fourfold increase in predator taxonomic diversity during the so-called Mid-Mesozoic Marine Revolution (Vermeij 1997; Bambach 2002),
An alternative macroevolutionary explanation for the relationship between adaptation and a changing biotic environment was proposed by Vermeij's (1987) hypothesis of escalation. Crediting the original idea to Darwin (1859), Vermeij (1987) states that even though species may not have experienced a net increase in fitness through adaptive evolution, their given biotic environment has become more rigorous across evolutionary time. Increasing biological hazards including competition and predation and an overall escalation of enemy-related adaptations to these hazards are the defining characteristics of this hypothesis. Escalation takes place when adaptations to a hazard become better developed over time. Like Van Valen (1973), Vermeij (1987) also turns to the fossil record to provide evidence for his hypothesis. He describes many instances of adaptive morphological and behavioral change from the Phanerozoic era that can be attributed to hazardous interactions between species. Examples include evidence of increases in the representation and power of shell-breaking marine predators, the prevalence of armor in gastropods and cephalopods, and the metabolic rates of suspension-feeding organisms (Vermeij 1987-add more refs???).
In the top-down view of escalation, enemies and competitors are the most important agents of selection due to the availability of resources. Resources necessary for survival are either organisms themselves, including mates and prey, or controlled by organisms, such as food and shelter. An individual's survival and fitness depends on acquiring and defending these resources, and those in control of the resources are also in control of the direction evolution (Vermeij 1987, Vermeij 1994). Through escalation, the minimum defense levels required for the purpose of obtaining or defending resources have increased over time in response to a consistently more competitive biotic environment. Some examples of adaptive defenses include armor, speed and agility, crypsis, and toxicity (ref???).
Escalation does not exhibit coevolution between enemy and victim, contrary to the reciprocal coevolution indicated by the RQH. Enemy driven evolution, also termed unilateral coevolution (Futuyma & Slatkin 1983), is essential to the hypothesis of escalation. Specifically in terms of predator-prey dynamics, prey respond to their predators, and rather than predators reciprocally responding to their prey, they are more likely to respond to their own enemies (Vermeij 1987). Because escalation lacks reciprocal evolution in response to prey species, arms races are not likely under this scenario.
Distinctions between escalation and the Red Queen
Selection pressures
The RQH and the hypothesis of escalation are similar in that they both emphasize the significance of biotic conflict rather than abiotic forces in driving the macroevolutionary trends of adaptive evolution. However, one of the major differences between the two theories is their view on the nature and direction of selective pressures in enemy-victim systems. Subsequently, the asymmetrical selection pressures experienced by predators and prey lead to different interpretations of a coevolutionary arms race. These distinctions have sparked much debate in the literature regarding which processes are responsible for influencing adaptive change (i.e. Dietl & Kelley 2002, Dietl 2003, Thompson 1999, Vermeij 2013).
The RQH emphasizes reciprocal selection on competing species in order to counteract changes in their biotic environment, while escalation occurs because of enemy-driven, top-down selective pressure where enemies evolve in response to their own enemies instead of reciprocally with their victims. However, both of these hypotheses favor directional selection, rather than stabilizing or disruptive selection, as phenotypes take on more extreme values over evolutionary time. While it may appear that two interacting predator and prey species are increasing a certain trait value, this is not enough evidence to imply escalation or Red Queen dynamics. Even though there might be a correlation between the morphological features of predator and prey, this does not necessarily infer reciprocal selection because you must look to the selective pressures taking place from the predator’s enemy (ref). For example, crabs of Lake Tanganyika in Africa, and their gastropod prey (West et al. 1991).
In addition to the direction of selection within the enemy-victim interactions, another important contrast is the differing magnitudes of selective pressure in predator-prey systems. In Red Queen dynamics, two interacting species are each other's strongest sources of selections, whereas in escalation, the strongest selective agent comes from enemies. The hypothesis of escalation also suggests that the strength of selection by enemies has increased over time as more dangerous biotic hazards have arisen (Vermeij 1987). Even prior to publishing the hypothesis of escalation, Vermeij (1982) noted that if predators prey on multiple species, the strength of selection on them is further decreased since they could preferentially prey on less-defended species. Indeed, many studies have found evidence that selection pressure by predators on prey is usually much stronger than selection by prey on predators (refs???). Evolutionary models suggest that prey will very likely evolve in response to predation, but predators don't necessarily respond to prey adaptations (Abrams 1986, Abrams & Matsuda 1996). Abrams (2000) also explains that because of the greater response of prey, they must evolve much faster than predators.
A potential reason why predators and prey experience asymmetrical selection pressures in their interactions may be because of the life-dinner principle (Dawkins and Krebs 1979). This principle explains that during an interaction between predator and prey, if the predator is unsuccessful in capturing the prey then it only loses its meal, whereas if the prey is unsuccessful it loses its life. As a result, selection on prey to evolve defenses is much stronger than selection on predators to evolve offensive capabilities (ref?). The life-dinner principle reinforces the hypothesis of escalation's enemy-driven selection, and challenges the idea of reciprocal coevolution of the RQH.
Coevolutionary arms races
As previously mentioned, the RQH and escalation both suggest different interpretations of the coevolutionary arms race analogy, leading to conflicting views of applying this idea to enemy-victim interactions. Due to the asymmetrical selection pressures experienced by predators and prey, they should not be considered equal partners in an arms race (refs???). Vermeij (1983, 1987, 1994) argues that escalation may only cause an arms race in the case of mutual enemies. Predators and dangerous prey, such as those with toxin secretions or spines, or hosts and parasites exert similar selection pressures on one another because they will both face risks during the interaction (Brodie & Brodie 1999). One of the best known examples of this is rough-skinned newts who possess a potent neurotoxin in their skin called tetrodotoxin, and garter snakes, who consequently evolve resistance to this toxin (i.e. Brodie & Brodie 1990, Brodie et al. 2004, Hanifin et al. 1999). In Red Queen dynamics, the reciprocal coevolution would potentially lead to a boundless arms-race scenario where prey defenses and predator counter-defenses cycle endlessly via directional selection, as seen in Figure 2. However, it is a false assumption that continuous adaptive evolution is possible (Vermeij & Roopnarine 2013). Rosenzweig et al. (1987) also highlights that an adaptive stalemate may be the most probably outcome of an arms race because conditions necessary for continuous evolution will rarely occur in nature.
Figure 2. Cycling of prey defenses (dashed line) and predator counter-defenses (solid line) under a coevolutionary arms race scenario. The units of the x and y-axes are arbitrary and depend on the specific system being studied. Adapted from Thompson 2005, page 91.
The questionability of predator-prey coevolutionary arms races could be due to the fact that selection on defenses or counter-defenses is only able to occur to a certain extent as a result of conflicting functional demands, trade-offs, and selective pressures experienced by an individual (Vermeij 1994). For example, a tortoise devotes much energy to developing its protective shell, but little energy goes to developing traits for speed and maneuverability. Other constraints to arms races include inefficient natural selection in small populations experiencing genetic drift and variation in the rate of appearance of beneficial mutations (Thompson 1986). Additionally, species will not invest in traits that may make them more vulnerable to other predators (Adler and Karban 1994 ???).
Applications to enemy-victim systems
As a result of the differences between the hypothesis of escalation and the RQH, the application of these theories to studies of real enemy-victim interactions varies. In general, escalation occurs when a species adapts due to interactions with their enemies, while Red Queen dynamics are common in host-parasite interactions and the evolution of sex (ref???). Most of the evidence originally used to defend these hypotheses comes from the fossil record (Van Valen 1973, Vermeij 1987). This is a valuable resource for studying adaptive evolution since it's the only source of long-term trends of interactions between species (Dietl & Kelley 2002). The examples of predator-prey interaction in the fossil record are usually more applicable to escalation, while Red Queen dynamics most often occur in hosts and parasites.
Many predator-prey systems that were once thought to experience reciprocal coevolution have since been reevaluated and are now considered examples of escalation. When referring to the extinction rates of the 25,000 subtaxa Van Valen (1973) originally analyzed, Vermeij even claims, "indeed, the data are also compatible with interpretations for escalation" (Vermeij 1994 p. 225). Shell drilling marine predators provide the foundation for many examples of escalation, and one notable example is naticid gastropods who would prey on molluscs. Initially, this system was hypothesized to be in a reciprocal coevolutionary arms race (Kitchell et al. 1981), but it was later stated that the fossil evidence actually indicates escalation (Kelley & Hansen 1996).
Examples of adaptive evolution… Vermeij (2008) also surveyed records to find 46 cases of marine organisms from the Mesozoic that showed evidence of adaptive innovations indicative of escalation.
Despite the lack of evidence for Red Queen dynamics in predator-prey interactions, the RQH has been widely applied to host-parasite interactions and the maintenance of sexual reproduction (i.e. Decaestecker et al. 2007, Howard & Lively 2002, Jokela et al. 2009, Lively 2010). Host-parasite coevolution is characterized by hosts only being resistant to certain parasite genotypes, while parasites can only infect a subset of host genotypes (Lively 2000, Little et al. 2006). Parasites preferentially attack the most common host genotypes, so they inherently favor clonal, asexual reproduction in their hosts (Thompson 2005). However, by producing offspring with rare genotypes through sexual reproduction, host lineages are more likely to escape infection by their coevolving parasites (Thompson 2005). Where sexual and asexual reproduction in a species is possible, asexual populations should only be found where coevolving parasites are uncommon or absent (Bell 1982, Lively & Jokela 2002).
Parasite-driven selection for sexual reproduction in hosts is thus evolutionarily maintained due to Red Queen mosaics in which selection favors locally rare host genotypes to counteract local adaptation in parasite assemblages (Thompson 2005). For example, in populations of the minnow Poeciliopsis monacha, both sexual and asexual forms coexist, and the individuals with the most common clonal genotype were found to have significantly higher parasite loads, indicating rare genotypes conferred a fitness advantage (Lively et al. 1990). Sexual reproduction is also commonly maintained with Red Queen mosaics in populations of snails, Potamopyrgus antipodarum, and parasitic trematodes where common clones are more prone to infection (i.e. King et al. 2009, Jokela et al. 2009, McKone et al. 2016). Additionally, the close association between hosts and parasites is evident in their parallel structured phylogenies (Page 1994, Page 1998). Example?
Concluding Remarks
Concluding that escalation is more widely applicable to the evolution of adaptation.
There are two major underlying themes of this
paper. Our first goal was to clarify the conceptual differences between coevolution and escalation. The major difference between the two processes is in the nature of selection (Vermeij, 1994). Escalation is enemy-driven evolution. In this view, the role of prey (with the exception of dangerous prey) is downplayed in arms races between predator and prey. In coevolution, prey are linked tightly to their predator and are thought to drive the predator’s evolution.
we must recognize that predator-prey interactions are complex systems and that multiple factors may influence the outcome of encounters between predator and prey.
Solutions to the conceptual conflicts between the coevolution and escalation processes fundamentally depend on growing collaboration among ecologists and paleontologists.
Overall, the RQH has a limited application when there is asymmetrical selection pressure between predator and prey, and escalation seems to be a better fit for this type of interaction. It is important for studies to incorporate the context of other species influencing the interactions in order to characterize which of the two processes might be responsible for adaptive evolution. Despite these ideas being widely discussed, there seems to be very few detailed studies that analyze the role of a predator’s enemies beyond the intimate interactions of predator and prey (Dietl and Kelley 2002). Even predator-prey models fail to include interactions beyond that of the predator and prey themselves (i.e. Abrams….)
The models by DeAngelis and his colleagues (21, 42, 43) assume a tight reciprocal linkage between predator and prey; yet, both predator and prey interact with a host of other species (17, 40). and in the system of drilling predators and bivalved prey for which these models were specifically designed. there is no evidence of reciprocal interaction.
Despite the impact the hypothesis of escalation and the RQH have had on adaptive evolutionary theory, they are faced with limitations.
Rqh adaptive evolution is constant over time while escalation does not imply any rates
RQH states that adaptive evolutionary trends are a result of competing species interactions in the deteriorating environment while escalation says its because of the increasing hazards over time.
Citations of ‘a new evolutionary law’ reveal a recent surge of interest in the RQ, mirrored by recent increases in the numbers of published studies on the RQH (electronic supplementary material, figure S1).
Our empirical knowledge of predator-prey evolution comes mainly from the fossil record (adaptive evolution)
Unlike the Red Queen Hypothesis, escalation is solely a macroevolutionary process. RQH places emphasis on species changes and escalation is biotic hazards as the cause for the trends observed in the fossil record.
Perhaps our most important current need in the study of coevolution is to make it a true evolutionary ecological science. We need to do much more than show that selection is acting on particular traits. We need to understand when, where, and how coevolution shapes the genetic structure of real populations, how it organizes and reorganizes the outcomes of interactions under different ecological conditions, how it molds and connects interactions across actual landscapes, and how it contributes to the ongoing organization of communities.
Scientific debates often end not in resolution but in confusion and indifference.
Important as the insights offered by coevolutionary models are, I believe the models miss the essential distinction between coevolution and escalation. Populations of species may have positive effects on one another, but such effects do not imply reciprocal evolution.
In short, progress in the study of evolutionary phenomena such as escalation can be made only if we explore the ecological and functional contexts in which organisms live and evolve.
Extras:
the RQH asserts that in response to a continually deteriorating biotic environment, an increase in fitness in one species causes a net decrease in the fitness of all other species in the environment (Van Valen 1973). Competing species therefore exhibit reciprocal selection on one another in order to counteract these changes in their environment and "run in place." On the other hand, the hypothesis of escalation emphasizes the increase in biological hazards over time, which are counteracted by increases in defensive adaptations in order to maintain access to and control of resources (Vermeij 1987). In escalation, enemy-driven, top-down selective pressure is a key factor, rather than reciprocal interaction between enemy and victim, due to the impact enemies and competitors have on the biological hazards.
Mutual enemies may include predators and dangerous prey or parasites and hosts. For predators, dangerous prey such as those with toxic secretions, venom, or spines impose a danger to their predators and are able to seriously harm or kill them, so they must respond adaptively to one another (Brodie and Brodie 1999). Parasites also risk their lives by engaging with a host, genotypes? (Thompson 1994, Thompson 2005).
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