Character displacement and the origins of diversity

Abstract

In The Origin of Species, Darwin proposed his principle of divergence of character (a process now termed "character displacement") to explain how new species arise and why they differ from each other phenotypically. Darwin maintained that the origin of species and the evolution of differences between them is ultimately caused by divergent selection acting to minimize competitive interactions between initially similar individuals, populations, and species. Here, we examine the empirical support for the various claims that constitute Darwin's principle, specifically that (1) competition promotes divergent trait evolution, (2) the strength of competitively mediated divergent selection increases with increasing phenotypic similarity between competitors, (3) divergence can occur within species, and (4) competitively mediated divergence can trigger speciation. We also explore aspects that Darwin failed to consider. In particular, we describe how (1) divergence can arise from selection acting to lessen reproductive interactions, (2) divergence is fueled by the intersection of character displacement and sexual selection, and (3) phenotypic plasticity may play a key role in promoting character displacement. Generally, character displacement is well supported empirically, and it remains a vital explanation for how new species arise and diversify.

Figure 1

Direct evidence of character displacement in medium ground finches, Geospiza fortis. Shown is the mean beak size (± 95% confidence intervals) for a population of G. fortis on an undisturbed Galápagos island. In 1982, the large ground finch, G. magnirostris, arrived on the island and began to compete with the resident population of G. fortis for seeds, especially in the dry season when food is limiting. By the time a severe drought struck in 2003, the population size of G. magnirostris had increased substantially. Character displacement in G. fortis occurred in 2004–2005 (arrow), when selection acting against large-beaked G. fortis lead to the evolution of greatly reduced beak size among G. fortis. Gray bar marks the 95% confidence limits on the estimate of the mean in 1973 to illustrate subsequent changes in the mean. Redrawn from Grant and Grant (2006).

Figure 2

Experimental evidence of character displacement in Mexican spadefoot toad tadpoles, Spea multiplicata. Spea tadpoles occur as (a) an omnivore ecomorph, which feeds on detritus on the pond bottom, and (b) a morphologically distinctive carnivore ecomorph, which feeds on, and whose phenotype is induced by, anostracan fairy shrimp. Plains spadefoot toad tadpoles, S. bombifrons, which are similar in morphology and diet, outcompete S. multiplicata for shrimp. (c) Presumably because of selection imposed by S. bombifrons, S. multiplicata have undergone character displacement in tadpole morph production, but the degree of this character displacement increases with increasing intensity of interspecific competition: S. multiplicata tadpoles whose parents were derived from populations that historically have had more contact with S. bombifrons possess the lowest propensities to produce carnivores, even when tadpoles from different populations are reared under common conditions, suggesting that these population differences in morph expression are canalized. (d) In contrast to the situation in sympatry, S. multiplicata derived from allopatry possess plasticity to produce both ecomorphs. Thus, these individuals can be used to experimentally evaluate whether the presence of S. bombifrons per se has caused the canalized differences in tadpole morph production observed between sympatric populations and illustrated in panel (c). Such experiments reveal that allopatric S. multiplicata tadpoles produce increasingly less carnivore-like tadpoles as the frequency of S. bombifrons is experimentally increased, mirroring the canalized shifts observed in natural populations. Data in (c) from Pfennig and Murphy (2002) and Martin and Pfennig (2010); data in (d) from Pfennig and Murphy (2002).

Figure 3

Experimental evidence that divergent natural selection disfavors those individuals that are the most similar to their competitor in resource use. (a) Mexican spadefoot toad tadpoles, S. multiplicata compete with a heterospecific, S. bombifrons, for anostracan fairy shrimp, which are often limited in natural ponds. Within natural populations of both species, individuals typically vary in their inherent propensity to eat shrimp. (b) When individual S. multiplicata tadpoles are housed with a single S. bombifrons tadpole, the more similar the two individuals are, the lower the growth of the focal S. multiplicata tadpole (regardless of which species ate shrimp faster). The curved line is a quadratic regression estimate of relative growth (a proxy for fitness) as a function of a focal S. multiplicata tadpole’s similarity in resource use to its S. bombifrons competitor, as measured by the time it took each individual to consume shrimp prey. Redrawn from Pfennig et al. (2007).

Figure 4

Evidence of reproductive character displacement, as revealed by exaggerated divergence in sympatry between two species of stag beetles from Southeast Asia (genus Odontolabis). In allopatry, O. mouhoti and O. cuvera are similar in body size, genitalia length, and coloration. In sympatry, these two species show exaggerated divergence in these characters, all of which have been implicated in mate acquisition. Beetles redrawn from Kawano (2003). Data from Kawano (2003).