Evolutionary innovations overcome ancestral constraints: a re‐examination of character evolution in male sepsid flies

In a recent article, Eberhard discussed whether the origin of morphological innovations is rare because of developmental constraints or whether their appearance is primarily driven by natural selection, and he argued in favor of the latter (Eberhard 2001). Eberhard’s reasoning is based on a study that traces the evolutionary origination of a major morphological innovation in a group of flies (Diptera: Sepsidae) using Meier’s (1995) phylogenetic hypothesis. The innovation consists of movable abdominal lobes in the males of this group, a character that is extremely rare in other flies. Eberhard also presented evidence that the appendages are used to stimulate the female during copulation. According to his preliminary character state reconstruction, this character originated two or three times in the clade of 240 species of flies. Eberhard concluded that abdominal lobes must evolve easily because there are multiple originations of this character within the sepsids. Thus, the ancestral lineage is inferred to be not constrained to produce the derived character. At issue in this study is a suggestion that we proposed in a 1991 review of the novelty concept (Müller and Wagner 1991). From a survey of examples from vertebrate evolution, we concluded that the lineage ancestral to a major innovation is developmentally constrained to acquire the derived character and that the rareness of innovations is explained by the need to overcome this ancestral constraint. If this is true, the study of innovations would have a different research agenda than the study of adaptation. This would justify recognition of innovation as a concept distinct from adaptation. A major research objective in the study of innovations would be to identify the developmental apomorphies that allowed the derived lineage to overcome the ancestral constraint (Prum 1999). Eberhard, however, concluded that his data refuted our suggestion and by implication would render the concept of innovations superfluous. As an alternative, he proposed that sexual selection is sufficient to explain the origin of this character in sepsids and the almost uniform absence of this character in other dipterans. A close examination of the facts presented in the article led us to conclude that the data do not support his conclusion. In contrast, we think that the data actually strongly support our suggestion that natural selection alone is not sufficient to explain the origination of morphological novelties. Later here, we outline the argument supporting this conclusion.