In this chapter I survey how biologists and paleontologists have used their imagination and evolutionary intuitions to animate phylogenetic narratives. Many authors intuited the direction of character evolution from clues provided by the threefold parallelism. The form changes that can be observed during ontogeny, and those inferred from the stratigraphic sequence of fossils, have inbuilt time axes that can be used as shortcuts for proposing lineages of changing forms. But interpreting the polarity of character change suggested by the systematic leg of the threefold parallelism was less straightforward. Many researchers intuited or imposed the direction of evolutionary change by proposing smoothly transitional linear series of observed or imagined forms. Some evolutionary intuitions date back to pre-evolutionary times, while others emerged from the search for evolutionary laws, such as Cope’s rule of phyletic size increase. When the first molecular phylogenies were published, researchers often muted their once vocal evolutionary intuitions to accept sometimes deeply puzzling results. The complete suppression of the evolutionary imagination is associated with the flawed but widespread strategy of using observed differences between taxa as prima facie evidence against monophyly and homology. It frequently diverts phylogenetic debates into fruitless avenues.

In this chapter I chronicle the emergence of different phylogenetic traditions in invertebrate zoology that coalesced around attractive hypothetical ancestors. The first half of the chapter discusses different scenarios for the origin of Bilateria that emerged in the late nineteenth and early twentieth centuries, including the enterocoel and archicoelomate theories, and the importance of the contested character of amphistomy for these scenarios. These scenarios became phylogenetic totems in different parts of the world, with Gastraea at the core of the European zoological tradition, and Phagocytella rooting both the Russian and American traditions. In the mid-twentieth century an alternative theory was proposed that derived bilaterians directly from ciliate ancestors. Remarkably, this attraction to ciliate ancestors emerged three times independently in quick succession, which illustrates the epistemic importance accorded to the precursor potential of hypothetical ancestors in narrative phylogenetic debates. The second half of the chapter discusses why many authors have felt so strongly attracted to annelid-like ancestors. These were proposed to have crawled at the cradles of many taxa, including molluscs, arthropods, vertebrates, and Bilateria. The arguments used to promote annelid-like ancestors form a conspicuous strand in the history of narrative phylogenetics, and it can still be traced today.

In this chapter I show that although hypothetical ancestors largely lost their epistemic power as deliberately constructed phylogenetic tools after the spread of modern phylogenetics, narrative phylogenetic reasoning persists. A conspicuous and widespread example of employing narrative shortcuts in evolutionary storytelling today is the attempt to use the phylogenetic position of taxa to predict the presence of ancestral character states. In close analogy to the historical use of the label ‘lower’ to designate taxa that are presumed primitive, modern authors use a range of evocative adjectives to promote the presumed presence of ancestral character states in their favoured taxa. ‘Basal’ is the most frequently used label, and many authors think that its link to the phylogenetic position of taxa gives it predictive power over whether these are likely to have retained ancestral states. I explain that phylogenetic and evolutionary theory provide no convincing rationale for this argument, and argue instead that basal taxa can be especially misleading about the nature of their character states. Proper lineage thinking can help one avoid this conceptual mistake.

In this chapter I discuss the anatomy of evolutionary storytelling. Historical narratives are woven around central subjects that lend them continuity through time. The central subjects of phylogenetic scenarios are lineages of hypothetical ancestors. These define the pathways of homology along which evolutionary change is reconstructed, and they root the power of phylogenetic hypotheses to explain the evolution of form by allowing characters in descendants to be traced back to ancestral precursors. De novo origins of novel traits are chinks in the explanatory armory of phylogenetic hypotheses. Hypothetical ancestors have therefore often been deliberately equipped with characters that provide suitable precursors of the traits that await evolutionary explanation. I will argue that the precursor potential of hypothetical ancestors functioned as an early phylogenetic optimality criterion used in the construction and judging of scenarios.

In this chapter I outline the transformation of systematics into phylogenetics by tracing the emergence of lineage thinking. One of the routes to a realist interpretation of the natural system of systematic relationships was to temporalize it. Lineage thinking emerged when the previously atemporal and symmetrical affinity relationships between contemporaneous taxa were replaced by asymmetrical ancestor-descendant relationships that tracked the arrow of time. This transition was accompanied by a rapid decrease in the diversity of shapes of affinity diagrams published in the systematic literature, and it marked a shift from predominantly reticulating or web-like systems to tree-like figures soon after the publication of Darwin’s On the origin of species in 1859. I argue that this graphic revolution largely records the influence of evolutionary expectations, as biologists redrew their diagrams to fit the theoretical dictates of Darwinian descent with modification. The current swell of enthusiasm for evolutionary networks has driven several recent authors to the peculiar argument that even Darwin disliked the tree of life as an evolutionary metaphor, an argument I will refute. Reconceiving the systematic relationships between taxa as phylogenetic pathways along which body plans evolve had an epistemic corollary. Speculation became a necessary tool for the evolutionary storyteller.

In this chapter I examine one of the earliest debates about animal body plan evolution. Ernst Haeckel, E. Ray Lankester, Francis Maitland Balfour, Elie Metschnikoff, and Otto Bütschli were the main participants in an international debate about the origins of animals that was triggered by the publication of Haeckel’s Gastraea theory in the 1870s. Each author proposed a different hypothetical animal ancestor, which, with the exception of Bütschli’s, were the products of recapitulationist reasoning. Each of these hypothetical creatures stood at the beginning of a unique scenario with a distinctive explanatory texture, and many of them can still be found in the pages of zoology textbooks today. This late-nineteenth-century clash of scenarios is representative of narrative phylogenetic debates generally. It shows how unique evolutionary stories are produced by authors wielding their personal evolutionary intuitions in the context of unequal attention to available evidence. Unsurprisingly, disagreements quickly became entrenched as dogma, but strikingly, several of these early scenarios, as well as their descendants, continue to inform current debates in the primary literature today.

In this chapter I trace the origin of the idea of evolutionary ancestors back to pre-evolutionary archetype concepts in the thinking of Johann Wolfgang von Goethe, Étienne Geoffroy Saint-Hilaire, and Richard Owen. Ancestors and archetypes were both used to explain unity of type, homology, and the origins of organismal form, but due to their metaphysical dissimilarity, they achieved this in fundamentally different ways. The archetypal thinking of these authors each illuminates a distinctive aspect of this explanatory strategy. I also diagnose and defuse a modern myth that has arisen about the views of Geoffroy Saint-Hilaire, which claims that he thought that the ventral surface of arthropods corresponds to the dorsal surface of vertebrates. When Darwin reinterpreted the archetype as an ancestor, evolutionary storytelling became possible, with hypothetical ancestors becoming the central subjects in phylogenetic narratives. But the emergence of ancestors as actors in evolutionary stories also required reconceptualizing the systematic relationships between taxa to provide pathways along which evolutionary stories could flow.

Finally, in this chapter I offer a concluding meditation on the undiminished value, indeed the necessity, of evolutionary storytelling, if our goal is to go beyond the trees and try to understand what may have happened along life’s myriad evolving lineages. As soon as one looks at a tree and asks ‘what does this mean?’, one becomes an evolutionary storyteller. Some dismiss such stories as pure fiction, and would prefer not to go beyond the tree. But for those of us who wish to peer over the phylogenetic frontier, these stories are how we generate our understanding of evolution, or at least how we try to.

In this chapter I address flaws in lineage thinking that are common in the professional, popular, and eductional literature, and which result from confusing the branching relationships between collateral relatives in the realm of systematics with the linear relationships between ancestors and descendants in the realm of evolutionary descent. The influential voices of the late Stephen Jay Gould and Robert O’Hara, who dubbed the now ubiquitous phrase ‘tree thinking’, have warned readers for decades against the sins of linear evolutionary storytelling and the use of linear evolutionary imagery. However, I argue that their impact has been deeply pernicious. The writings of Gould and O’Hara fundamentally misconstrue the relationship between the branching realm of systematics and the linear realm of evolving lineages. I close with a discussion of the problem that, in the absence of a vocabulary designed to talk about lineages, we are forced to discuss them in the taxic language of systematics. This inevitably causes problems.