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 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 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.