The erratic and contingent progression of research on territoriality: a case study

Our understanding of animal mating systems has changed dramatically with the advent of molecular methods to determine individuals' reproductive success. But why are older behavioral descriptions and newer genetic descriptions of mating systems often seemingly inconsistent? We argue that a potentially important reason for such inconsistencies is a research trajectory rooted in early studies that were equivocal and overreaching, followed by studies that accepted earlier conclusions at face value and assumed, rather than tested, key ideas about animal mating systems. We illustrate our argument using Anolis lizards, whose social behavior has been studied for nearly a century. A dominant view emerging from this behavioral research was that anoles display strict territorial polygyny, where females mate with just the one male in whose territory they reside. However, all genetic evidence suggests that females frequently mate with multiple males. We trace this mismatch to early studies that concluded that anoles are territorial based on limited data. Subsequent research assumed territoriality implicitly or explicitly, resulting in studies that were unlikely to uncover or consider important any evidence of anoles' departures from strict territorial polygyny. Thus, descriptions of anole behavior were largely led away from predicting a pattern of female multiple mating. We end by considering the broader implications of such erratic trajectories for the study of animal mating systems and posit that precise definitions, renewed attention to natural history, and explicitly questioning assumptions made while collecting behavioral observations will allow us to move towards a fuller understanding of animal mating systems. Significance statement Mismatches between behavioral and genetic descriptions of mating systems are widespread across animals. We argue that these discrepancies can arise from the erratic and contingent progression of research on space use behavior and social interactions. We demonstrate such a trajectory in Anolis lizards, where decades of behavioral data led not only to the conclusion that anoles are territorial but also to the erroneous expectation, disproven by genetic evidence, that each female mates with just one male. The earliest studies concluded that anoles are territorial based on flimsy evidence, leading subsequent studies to implicitly and explicitly assume territorial behavior; later studies were thus unlikely to detect, or consider important, departures from territoriality that could facilitate female multiple mating. Such research trajectories are likely not unique to anoles, and we contend that avoiding these trajectories requires renewed and continued attention to the natural history of even well-studied organisms.