The Princeton Guide to Evolution

VI.15

Key Evolutionary Innovations

Michael E. Alfaro

OUTLINE

1. Key innovation concepts in evolutionary biology

2. Where do key evolutionary innovations originate?

3. How do key innovations lead to evolutionary diversity?

4. Testing hypotheses of key innovation

5. Problems with the idea of key innovations

Biologists have long suspected that evolution of traits with strong ecological significance fuels rapid diversification in both species formation and phenotypes. New tools and advances in macroevolutionary theory have helped clarify how key evolutionary changes are expected to affect diversification. Empirical studies often reveal that the relationship between key traits and evolutionary does not conform to simple expectations.

GLOSSARY

Adaptive Zone. A set of closely related niches exploited in a similar manner by a lineage that has evolved a key trait.

Clade. All the descendants of a common ancestor in a phylogenetic tree.

Comparative Method. A statistical method for comparing traits of lineages that incorporates phylogenetic relatedness.

Diversification. An increase in species richness or morphological diversity within a clade.

Ecological Opportunity. A set of niches newly available to a lineage experiencing adaptive radiation.

Exaptation. A trait that arose via natural selection for one function and was then co-opted for a new function by a change in selective pressure.

Key Evolutionary Innovation. A trait or functionally related series of traits of outstanding ecological significance that is thought to have contributed to either the species richness of a lineage or its ecological diversity, or to both.

Lineage. A series of species connected by ancestor-descendant relationships.

Sister Clade. The clade most closely related to (sharing a most recent common ancestor with) a focal clade.

1. KEY INNOVATION CONCEPTS IN EVOLUTIONARY BIOLOGY

With more than 10,000 species distributed across the world in most major habitats, birds are widely considered a story of evolutionary success. Can this success be tied to a key evolutionary feature of the lineage like wings or powered flight? This is the essence of the key evolutionary innovation hypothesis in macroevolution, which posits that exceptionally diverse lineages owe their evolutionary success to the evolution of a small number of traits of great ecological or functional significance.

The idea of key innovations has a long history in evolutionary biology. Originally, the term was used to describe the ecological traits believed to be most important in producing higher taxonomic groups. Thus, wings might be proposed as a key innovation for the order Aves (birds), while hardened scales and elongate tongues might be suspected as key innovations explaining the origin of pangolins—a much smaller clade containing only eight species. Such use of the term emphasizes evolutionary distinctiveness rather than species richness. Despite their low species richness, pangolins are phenotypically unique from other lineages of mammals owing to key traits such as an elongate tongue and keratin scales that, presumably, allow them to persist in a unique adaptive zone even if the zone does not permit the same level of species diversification as do wings.

Modern uses of the term key evolutionary innovations treat them as traits that confer exceptional evolutionary “success” to a lineage, but biologists differ in their definitions and measures of success. The great disparity in patterns of species richness is perhaps the most pervasive feature of the tree of life, and much of the research on key innovations over the last 20 years has centered on testing whether key traits can explain why some lineages have evolved so many species. Under this conception of evolutionary success, key traits provide a fitness advantage to the lineage itself, leading to higher rates of speciation and/or lower rates of extinction compared with related lineages that lack the trait. Key innovations in this context are a mechanism for driving species selection (see chapter VI.14). With the emergence of a more rigorous theoretical framework for studying adaptive radiations (see chapter VI.10), biologists have recently focused on the expected link between ecological adaptive radiation and the evolution of traits associated with novel niches. As a result, more recent studies of key innovations sometimes define evolutionary success as the degree of morphological and ecological diversity within a lineage. The section “Testing Hypotheses of Key Innovation” explores this idea in greater detail.

The scale at which key evolutionary theory is applied is flexible. Bird wings, mammalian hair, and the amnion of terrestrial vertebrates are all examples of key traits that have been suggested as underlying the success of vast radiations. However, key traits are also used to explain radiations at much smaller scales. The evolution of grinding pharyngeal jaws has been suggested as the key trait underlying a radiation of about 90 species of herbivorous parrot fish, while several traits associated with mouthbrooding have been suggested to be innovations that allowed diversification of lake-dwelling haplochromine cichlids in Africa within the last 8 million years. The important point for modern evolutionary biologists is that the acquisition of key traits at any scale is predicted to alter the tempo of evolutionary diversification.

It is often said that key innovations are easy to propose and hard to test! Interesting key innovations that have been proposed include flowers as the key trait that enabled the astonishing diversification of living angiosperms; the evolution of phytophagy (plant feeding) as underlying success in several insect lineages, including species-rich clades of beetles; powered flight as underlying the success of bats, birds, pterosaurs, and flying insects; and bipedalism as underlying the evolutionary success of hominids. Hundreds more examples can be found within the primary literature on evolutionary biology, although the number of studies that critically test this hypothesis is much smaller. This chapter focuses on the role of key evolutionary innovation in explaining patterns of biodiversity: how evolutionary success is measured, how key innovations are thought to contribute to this success, and what problems are associated with the application of theory to empirical data sets. The concept of key evolutionary innovation has played an important role in shaping the kinds of questions that biologists ask and challenged them to find new ways to test these appealing but often vexing explanations of biodiversity.

2. WHERE DO KEY EVOLUTIONARY INNOVATIONS ORIGINATE?

The concept of key innovations has been applied to both simple and complex changes in a trait. In some cases, a small change in a character can allow a lineage to cross a major functional or ecological threshold. For example, a mutation leading to a single amino acid substitution may confer resistance to a toxin or pathogen and allow a lineage access to a previously unavailable habitat, or a small increase in jaw muscle size may allow a predator to crack shelled prey. Other proposed key innovations are more complicated. Powered flight in birds relies on several proposed key traits, including wings and feathers. Wings themselves are complex structures that comprise heavily modified forelimbs, including the elongation of a reduced number of digits; a specific arrangement of feathers; and physiological and behavioral changes to support flight. This trait really represents a large collection of changes from the ancestral phenotype. When the key innovation represents a suite of functionally related characters, the evolution of the key trait may involve the co-opting of characters that arose under natural selection for a different function. For example, because feathers are found on many species of flightless, nonavian theropod dinosaurs, the origin of feathers cannot be explained as an adaptation for flight. Instead, it is likely that feathers initially evolved for insulation and/or display. The asymmetrical, highly modified feathers found on the wings of modern birds resulted from a shift in selective pressure from this ancestral function to satisfy new demands associated with powered flight. Traits that have experienced functional shifts over their evolutionary history in this way are called exaptations (see chapter II.7). Other anatomical changes associated with flight such as modifications to the forelimb and pectoral girdle similarly represent the co-opting of existing structures to novel functional demands. The evolution of a key innovation may thus represent several important evolutionary steps that lead to ever-increasing functional ability. Once a sufficient number of traits have evolved to allow a lineage to fully enter a new adaptive zone, the rate of evolutionary diversification is expected to increase.

3. HOW DO KEY INNOVATIONS LEAD TO EVOLUTIONARY DIVERSITY?

It is readily apparent that certain traits confer large ecological advantages. Wings allow birds access to habitats that are out of reach to most flightless predators and competitors and provide a means of rapid escape as well as a way to quickly reach new habitats if local conditions become unfavorable. How might these ecological advantages translate to evolutionary success? Biologists historically recognize three avenues. Traits might allow a lineage to exploit a new adaptive zone—a set of related niches that can be filled only by species possessing an evolutionary novelty such as wings. Second, novel traits might confer a competitive advantage on species possessing it, allowing a lineage to drive competing species to extinction. Fish lineages that evolve the ability to protrude their jaws might enjoy a greatly improved ability to capture prey using suction feeding. On ecological timescales, this trait might result in populations of jaw-protruding species that owing to a competitive advantage in exploiting food resources, are larger than populations of species that lack the trait. Since smaller populations are more vulnerable to extinction, species within lineages lacking the trait might go extinct at a faster rate than those with jaw protrusion. At evolutionary timescales, this sequence could lead to a proliferation of species with the key innovation (see discussion of species selection in chapter VI.14). A third way in which an innovation could produce evolutionary success is by increasing the potential for reproductive isolation and species formation. The evolution of complex mating behaviors within a lineage, for example, might lead to increased potential for speciation between geographically isolated populations and cause the species richness of that lineage to increase.

The ecological theory of adaptive radiation also provides a link between key innovations and evolutionary success. An ecological adaptive radiation is the rapid evolution of morphological differences and species richness in a closely related group (see chapter VI.10). Adaptive radiations are spurred when a lineage gains access to ecological opportunity—the potential to diversify into new niches along a similar ecological axis. Within the framework of ecological adaptive radiation theory, key innovations can be thought of as traits that grant a lineage ecological opportunity by allowing them to reach a new adaptive zone. As an illustration of these ideas consider the evolution of algal grazing in fish. Algal grazing has evolved in several lineages of marine and freshwater fish including parrot fish, surgeonfish, damselfish, and cichlids, and each of these lineages exhibits conspicuous adaptations of the skull and jaws that are presumably key traits associated with this lifestyle. Niches associated with grazing on algae are likely unavailable to closely related fish lineages that nevertheless lack modified jaws to efficiently scrape algae from rocks or reefs. Once lineages evolve these traits (the key innovations), they gain ecological opportunity and enter a new adaptive zone related to herbivory. Freed from competition with other species for food, the member species of the algal-feeding lineage may initially invade new habitats. Diversification within this lineage may follow an ecological axis as formerly geographically isolated populations that come back into contact evolve reduced competition by specializing on different types of algae or on algae that grow at different depths. Given time, the colonizing species diversifies into a radiation characterized by a unique ecology enabled by a key trait.

One difficulty with many key innovation hypotheses lies in linking the key trait to the process of diversification. Some suggested key innovations play an obvious role in species recognition, and it is relatively straightforward to envision how evolution of the trait would lead to higher rates of speciation. One of the best-documented examples of a key evolutionary trait is the nectar spur of columbines (genus Aquilegia). Scott A. Hodges and Michael L. Arnold have statistically demonstrated that the rate of diversification of columbines and other plant lineages with nectar spurs is higher than for those lacking this trait. Additional studies have shown that nectar spur length influences the kinds of pollinators that will visit a flower and that the evolutionary association between pollinators and flowers reflects evolutionary change toward longer spurs as well as shifts to pollinator species with longer tongues. Research on this system supports the hypothesis that nectar spurs have affected both reproductive success and reproductive isolation of the species that possess them, providing a link between the macroevolutionary pattern of high diversity for lineages with the key trait and microevolutionary mechanisms relating directly to the trait that could lead to this diversity For these reasons, the nectar spurs of Aquilegia species constitute one of the best-documented examples of a key evolutionary innovation.

Unfortunately, most other suggested key innovations are not so obviously linked to reproductive isolation. In the example of algal grazing in fish, although the ecological significance of scraping jaws for an algae-feeding fish is clear, it is less clear how a trait that is associated with feeding could lead to increased rates of reproductive isolation. One possibility is that key traits not obviously linked to reproductive isolation may still increase species diversification by making either the formation or survival of geographically isolated populations more likely through the ecological advantages they confer. For example, latex and resin canals are defensive structures that have evolved independently in many plant lineages, including conifers, mulberries, and daisies. They are hypothesized to be key innovations that protect plants from pathogens and predators, and Brian D. Farrell and colleagues have shown that lineages with resin canals tend to have a much larger number of species than closely related lineages lacking them. Although this trait is not an integral part of the mating system, as are nectar spurs, they may still turn the engine of species formation by allowing isolated populations to persist at a higher rate than populations without resin canals. A greater frequency of isolated populations, in turn, would be expected to lead to a higher rate of evolution of reproductive isolation within these populations, leading to more species. In support of this idea, Farrell and colleagues have shown at one field site that species with latex and resin canals are more numerically abundant than those without them. This evidence is only suggestive, however, and illustrates that nearly all proposed key evolutionary innovations, including persuasive examples like resin canals, lack an explicit mechanism that demonstrates how the trait gives rise to observed diversity.

4. TESTING HYPOTHESES OF KEY INNOVATION

If key innovations promote evolutionary success, then a simple prediction of key innovation hypotheses is that lineages with the traits should be more successful than closely related lineages lacking them. Success is most commonly measured by the number of species, but more recently, workers have also measured the richness of morphological or ecological diversity contained within a lineage. To assess differences in species richness, biologists often use sister clade comparisons, which involve counting the number of species within the lineage that have evolved the trait versus the number of species in the sister clade, the most closely related lineage lacking the purported innovation. One problem with simple counts lies in judging the statistical significance of the difference. If the lineage with the key trait has 20 species and its sister clade contains 5, is the magnitude of the difference sufficiently large to support the key innovation hypothesis? To answer this question, biologists have turned to stochastic models of diversification such as the birth-death model, which treats speciation and extinction as random events controlled by fixed rates of species birth and death (see chapter VI.11). Because the diversification process is probabilistic, sister lineages that have evolved under identical rates of speciation can nevertheless differ in the number of species they contain. These stochastic models form the basis for determining when the difference in species richness between two lineages is so great that it is unlikely they share a single diversification rate. The most compelling tests of key innovation use these methods in conjunction with large-scale phylogenies in which the proposed innovation has evolved multiple times. For example, Farrell has shown that the diversification rate of angiosperm-feeding beetle lineages is significantly higher than that of other phytophagous lineages, which suggests that angiosperm feeding is a key evolutionary innovation for beetles. Hodges and Arnold took a related approach to show that the diversification rate of nectar-spur-bearing plant lineages is significantly higher than that of lineages lacking the trait. The statistical rigor of the comparisons in these studies and the distribution of the key trait over many independent lineages have helped make phytophagy and the latex-resin systems currently two of the most widely accepted examples of key evolutionary innovation in evolutionary biology.

The ecological theory of adaptive radiation has facilitated the testing of key innovation hypotheses by furnishing two main predictions about the tempo of diversification in a lineage that has evolved a key novelty. One is that a lineage should show an increase in the rate of species formation following the acquisition of the key trait. This prediction stems from the idea that key innovations grant a lineage access to new niches. The other is that the rate of evolution of ecological traits related to the innovation should also increase, because diversification in the new adaptive zone is expected to occur along an ecological axis. Both predictions are similar in that they link key innovations to an expected increase in the tempo of evolutionary diversification.

The rise of molecular phylogenetics, which seeks to reconstruct the evolutionary history of taxa using DNA sequence data, combined with recent development of new comparative statistical methods for analyzing data in the context of a phylogeny, has fueled recent work on key innovations. Phylogenetic trees provide at least three important services in the study of key innovations. First, by looking at the distribution of a suspected key trait across all members of a clade in the context of their phylogeny, biologists can infer the time of origin of the trait. This information can be used to assess whether the timing of the appearance of the novelty is consistent with other events that are thought to play a role in allowing the diversification of the lineage. For example, if a key trait is thought to enable a lineage to exploit a new habitat, the age of origin of the trait can be compared with the fossil or paleoclimatic record to determine whether diversification patterns are consistent with the historical availability of that environment.

Second, molecular phylogenies provide a record of the tempo of all the speciation events that gave rise to the present-day members of a lineage. Since key innovations are expected to increase the rate of speciation, a phylogenetic tree can be used to ask directly whether speciation events occur at a faster rate following the acquisition of a key trait. The same is true for the rate of evolution of ecological traits.

Third, phylogenies can be used in conjunction with information about trait diversity within a clade to test whether the tempo of evolution of certain characters changes in a way that is consistent with the key innovation hypothesis. For example, suppose a novel joint between bones in the jaws of fish is thought to underlie the evolution of new and specialized feeding morphologies. If the jaw joint is the key innovation, one would predict that jaw elements related to feeding would be subject to new selective pressures as part of an ecological adaptive radiation spurred by the evolution of the trait. Thus, evolutionary rates of jaw characters should increase shortly after the evolution of the jaw joint. If jaw characters are shown to change more rapidly before the key trait appears, or if the tempo of jaw characters is the same before and after the evolution of the key trait, then the key innovation hypothesis would not be supported. A second prediction might be that the rate of evolution in characters unrelated to the key innovation, perhaps tail shape, should not differ between lineages with and without the presumed innovation. The power of comparative methods for testing historical hypotheses explains why these approaches have emerged as one of the primary ways of evaluating key innovation hypotheses in modern evolutionary biology.

5. PROBLEMS WITH THE IDEA OF KEY INNOVATIONS

Key innovations are sometimes criticized as being little more than evolutionary just-so stories. The idea that wings are the key to the success of birds may seem reasonable, but an expectation of how wings would have shaped the radiation of birds is needed to rigorously evaluate whether the available data support the hypothesis. Phylogenetic hypothesis testing in conjunction with the ecological theory of adaptive radiation has been extremely useful in addressing some of these criticisms. The ecological theory of adaptive radiation generates predictions (i.e., rates of speciation and/or morphological evolution should increase following the acquisition of a key trait), and phylogenetic methods, in conjunction with a phylogeny and data about the distribution of the putative innovation, provide a means for testing these predictions.

A difficulty with evaluating key innovation hypotheses is that the innovations often have evolved only a small number of times. In the case of a single large radiation, a comparative method may reveal that one lineage has a significantly greater number of species than its sister clade. This is the case with living birds, whose species richness and phenotypic diversity dwarfs that of the 24 species of crocodilians, their closest evolutionary cousins. It will generally not be possible, however, to identify one trait as the causal factor of the radiation over another if those traits are codistributed. For example, whereas a functional morphologist might see changes to the jaws as the key innovation, a physiologist might argue that it is the evolution of a novel biochemical pathway to process new foods. If both are inferred to evolve in the same ancestor of a clade, comparative methods alone will not be enough to tease these explanations apart, since they make identical predictions about the timing of a change in the tempo of diversification. When presumed innovations have evolved multiple times within a large phylogenetic tree, the ability to discriminate among competing putative innovations may be much improved. As long as the hypothesized innovations are not identically distributed across the tree, they will make different predictions about when the tempo of diversification will change. The weight of evidentiary data in support of one explanation versus the other can then be assessed with statistical methods. In the case of nectar spurs, Hodges and Arnold showed that the diversification rate of Aquilegia is significantly faster than in their sister clade. Although the authors attributed this difference to the nectar spur, one might argue that any other traits that evolved in the common ancestor of Aquilegia could have driven the radiation. However, additional comparisons of diversification rate in other plant lineages with nectar spurs with sister taxa lacking them allowed Hodges and Arnold to argue persuasively that the nectar spur itself is the innovation.

Biologists often suggest that key innovations underlie patterns of highly uneven species richness, yet the number of rigorous, phylogeny-based tests of the hypothesis is much smaller than the number of times key innovations have been proposed. Over the last 15 years, the concept of key innovation has been invoked in close to 400 articles within evolutionary biology, yet fewer than 10 percent of these articles tested these ideas with rigorous phylogenetic comparative analysis. And what do these phylogeny-based tests reveal about key innovations? Many studies (including those already discussed examining nectar spurs and angiosperm feeding) are able to quantify a difference in the rate of diversification between lineages that possess a trait and those that do not, providing evidence that key traits are linked to at least some of the major patterns of uneven diversity found on the tree of life. Furthermore, some studies have shown that purported key traits do not, in fact, produce exceptionally diverse groups. N. Ivalú Cacho and colleagues provide one such example, showing that extraflorally derived nectar spurs of some euphorbs have not led to exceptionally diversity within those lineages that possess them. Even when significant changes in diversity are detected, it is also common to find that shifts in the evolutionary rate of speciation or character evolution occurred somewhat later than the origin of proposed innovations. This is especially true for ancient innovations that characterize major taxonomic groups. Duane McKenna and colleagues found that major episodes of diversification within weevils, one of the most species-rich groups of angiosperm-feeding beetles, occurred 20–30 million years after weevils first colonized flowering plants. Another example concerns the role of genome duplication in fish diversification. Although the evolutionary success of teleosts—which constitute more than 99 percent of living fish—is sometimes linked to a duplication of the entire genome early in teleost history, Francesco Santini and colleagues have shown that most teleost diversity was produced by radiations within lineages that are much younger than the age of this hypothesized key innovation. This result reveals that the present-day species richness of teleosts is more likely to be the result of factors specific to these younger radiations than to the ancient genome duplication event. Phylogenetic approaches have also revealed many instances in which an innovation triggered a radiation in one lineage but not in others. Pharyngeal jaws (a second set of jaws in the throat of some fish) have been proposed as key innovations that underlie the species richness of wrasses (~600 species), damselfish (~360 species), and cichlids (~2000+ species). Yet the surfperches, which have also evolved modified pharyngeal jaws, contain a much smaller number (only ~60 species), suggesting that the trait itself does not always lead to a burst of speciation. Rigorous and explicit tests of the pharyngeal jaws as a key innovation hypothesis using sister clade comparisons or other phylogenetic methods are impeded by the lack of a reliable phylogeny detailing relationships among fish families.

Explaining these apparent exceptions to the predictions of key innovation hypotheses remains an active area of macroevolutionary biology. One possibility is that diversity patterns in large groups have been influenced by more recent events that mask the signal of the initial radiation. Passerines, which include more than 60 percent of extant bird diversity, evolved almost 40 million years after the common ancestor of living birds. The pattern of diversification of this diverse, young group in conjunction with extinction of ancient bird lineages may swamp the signal for the tempo of diversification during the origin of modern birds. Without accurate inference of the pace of early bird diversification, the ability of phylogenetic comparative methods to test key innovation hypotheses will be extremely limited. The “drowning out” of the signal of the tempo of ancient radiations by more recent bursts in the tree may be common for large groups (e.g., beetles, mammals, teleost fish, birds), complicating the study of key innovations. In such cases, the key trait may ultimately be responsible for the initial evolutionary success of the group, but it does not explain some or most of the patterns of diversity that have evolved since the trait was acquired. The ability of simple key innovation hypotheses to explain biodiversity patterns in ancient groups may be severely limited, since richness in these cases will be the outcome of a series of complex historical factors.

A conceptual weakness of key innovation concepts is that they place a great deal of emphasis on the trait itself, whereas there is good reason to expect that the ecological and evolutionary context of the trait is likely to be important as well. Stronger jaws may allow cracking of hard-shelled prey, but evolutionary specialization in sense organs may also be needed to locate prey, or locomotor adaptions may be needed to forage in areas with high abundances of hard-shelled prey. Furthermore, stronger jaws may provide an evolutionary advantage only to lineages that first evolve them within an ecological community. The potential for diversity may also be a function of geography. For example, the geographic area available to an island-dwelling lineage that has evolved a functional innovation may be too small to support more than a few species. In this case the evolutionary potential of the innovation will go unrealized until the lineage is able to colonize a new, larger island or to recolonize the mainland.

To accommodate the idea that the evolutionary response to a proposed key trait may depend on other traits as well as on the ecological and historical context in which the trait is acquired, some biologists suggest that key innovations do not appear all at once in an ancestral species. Rather, key innovations are the outcome of several functional novelties that accumulate over a period that spans multiple ancestral species. Diversification and radiation begin once all the needed traits have evolved and other mitigating conditions are favorable. Testing these conceptions of key innovation is more difficult than testing the simple prediction that diversification rates immediately change once the key trait evolves, because most phylogenetic statistical methods are designed to locate single points on a phylogeny where the diversification rate abruptly shifts. It is still possible to make and test the more general prediction—that the key trait evolves some time before the change in diversification occurs; however, if a clade experiences any pulse of diversification subsequent to the origin of the key trait, it may be difficult to determine whether that pulse represents the end of the lag period and the start of a key trait-fueled radiation or a diversification driven by another, unrelated factor.

Despite these difficulties, the concept of key innovations remains important to macroevolution because it is a theoretical framework that links aspects of ecology to evolutionary patterns of biodiversity. Testing key innovations is not as hard as it once was, but it is apparent that the relationship between diversity and innovation is often complex, while available stochastic models of diversification used for testing are still relatively simple. The trend among researchers toward generating more explicit models of the evolution of key traits and expected patterns of lineage diversification given these models is certain to continue. As more sophisticated methods and better phylogenies for major sections of the tree of life become available, it will become increasingly possible to understand the role that trait innovation plays in generating diversity relative to other macroevolutionary factors like geographic distribution and interactions with other species.