The meaning of Darwin's 'abominable mystery'

Am J Bot. 2009 Jan;96(1):5-21. doi: 10.3732/ajb.0800150. Epub 2008 Dec 11.

Abstract

Charles Darwin's "abominable mystery" has come to symbolize just about all aspects of the origin and early evolution of flowering plants. Yet, there has never been an analysis of precisely what Darwin thought was so abominably mysterious. Here I explicate Darwin's thoughts and frustrations with the fossil record of flowering plants as revealed in correspondence with Joseph Hooker, Gaston de Saporta, and Oswald Heer between 1875 and 1881. I also examine the essay by John Ball that prompted Darwin to write his "abominable mystery" letter to Hooker in July of 1879. Contrary to what is generally believed, Darwin's abominable mystery has little if anything to do with the fossil prehistory of angiosperms, identification of the closest relatives of flowering plants, questions of the homologies (and character transformations) of defining features of flowering plants, or the phylogeny of flowering plants themselves. Darwin's abominable mystery and his abiding interest in the radiation of angiosperms were never driven primarily by a need to understand the literal text of the evolutionary history of flowering plants. Rather, Darwin was deeply bothered by what he perceived to be an abrupt origin and highly accelerated rate of diversification of flowering plants in the mid-Cretaceous. This led Darwin to create speculative arguments for a long, gradual, and undiscovered pre-Cretaceous history of flowering plants on a lost island or continent. Darwin also took refuge in the possibility that a rapid diversification of flowering plants in the mid-Cretaceous might, if real, have a biological explanation involving coevolutionary interactions between pollinating insects and angiosperms. Nevertheless, although generations of plant biologists have seized upon Darwin's abominable mystery as a metaphor for their struggle to understand angiosperm history, the evidence strongly suggests that the abominable mystery is not about angiosperms per se. On the contrary, Darwin's abominable mystery is about his abhorrence that evolution could be both rapid and potentially even saltational. Throughout the last years of his life, it just so happens that flowering plants, among all groups of organisms, presented Darwin with the most extreme exception to his strongly held notion natura non facit saltum, nature does not make a leap.