In the years following the publication of On the origin of species
), Darwin turned to the completion of his book On the various contrivances by which British and foreign orchids are fertilised by insects
), in which he exposed the functional significance of many of the intricacies of orchid flowers. Although the German botanist Konrad Sprengel had published an account of the function of flowers nearly 70 years earlier (Sprengel 1793
), it was Darwin who first fully recognized that hermaphrodite flowers had been shaped by natural selection largely to enhance cross-fertilization and to avoid selfing. His observations led him to conclude in Orchids
the inference that nature ‘abhors perpetual self-fertilization’ (p. 359).
Fourteen years later, Darwin published the results of experiments conducted in his ‘hothouse’ at Down: The effects of cross and self-fertilisation in the vegetable kingdom
). These experiments were largely motivated by a search for why natural selection had repeatedly favoured characters in plants that ensured crossing and prevented inbreeding, but Darwin was possibly also influenced by his anxiety that his marriage to his cousin, Emma Wedgwood, might have been responsible for the poor health of his children (Jones 2008
). Ultimately, however, it was serendipity that got him started: he noted after selfing and crossing individuals of the toadflax Linaria vulgaris
, ‘[f]or the sake of determining certain points with respect to inheritance’ (Darwin 1876
, p. 9), that the selfed progeny performed less well than the crossed.
Darwin repeated the comparison of inbred and outbred individuals for numerous other plant species by pitting selfed versus outcrossed progeny against one another in carefully controlled experiments. He documented inbreeding depression under a range of experimental conditions and recognized that its expression depends very much on the environment under which progeny are grown. The environmental dependency of inbreeding depression is now well established (e.g. Dudash 1990
) and may contribute to the maintenance of intermediate outcrossing rates in plants (reviewed in Goodwillie et al. 2005
). In the course of his experiments, Darwin (1876)
also stumbled upon what we now recognize as self-incompatibility. Intriguingly, although he recognized the adaptive significance of morphological traits that prevent selfing, he viewed self-infertility as somehow an ‘incidental’ trait with no obvious adaptive significance (p. 346).
Without our modern understanding of genetics, it is hard to imagine how one might explain inbreeding depression; Darwin's (1876)
explanation, which invoked an intrinsic advantage of crossing between individuals with somewhat divergent phenotypes, was thus understandably vague. Nor could Darwin explain his observation of what we would call the purging of inbreeding depression. Nonetheless, by subjecting his material to multiple generations of artificial selfing, he almost certainly discovered the phenomenon long before it was clearly confirmed in more recent times (Barrett & Charlesworth 1991
). After six generations of selfing and crossing lineages of the plant Ipomoea purpurea
, he noted that one selfed lineage became stronger than all the others. Amusingly, he referred to this lineage as ‘the Hero’, ‘which after a long and dubious struggle conquered its crossed opponent, though by only half an inch’! (Darwin 1876
, p. 47).
Darwin's observations convinced him that self-fertilization was intrinsically deleterious. However, he also recognized that the ability to self in the absence of mates could be an advantage, noting that hermaphrodites might benefit from ‘occasional or frequent self-fertilization, so as to ensure the propagation of the species, more especially in the case of organisms affixed for life to the same spot’ (Darwin 1876
, p. 462). The selection of self-fertile hermaphroditism for reproductive assurance is now widely accepted as responsible for the breakdown of self-incompatibility or the evolution of hermaphroditism from dioecy in many plant and animal species (Eppley & Jesson 2008
), particularly those with a history of long-distance dispersal (Baker 1955
Yet Darwin could not believe that complete selfing in the absence of any outcrossing could be maintained in the long term. His intuition is borne out by the fact that even habitual selfers, such as the model species Arabidopsis thaliana
, do occasionally outcross and show evidence in their genomes of recombination and its benefits (reviewed in Wright et al. 2008
). For instance, a small amount of outcrossing in habitual selfers probably accounts for the relatively rapid decline in linkage disequilibrium across the genome and is sufficient to overcome the negative implications of what would otherwise be an absence of effective recombination, such as the accumulation of deleterious mutations and a slowdown in the rate of adaptation (reviewed in Wright et al. 2008