Selective pressures on pollinator tongues and tubes are not uniform across geographic landscapes because interacting organisms seldom have precisely overlapping distribution ranges (Grant and Grant 1965). As a result, plants may have different floral visitors in different populations, and floral visitors may forage from different plant communities in different parts of their range. For example, Gomez et al. (2009) found that the mustard Erysimum mediohispanicum has very different pollinator communities in different populations and that this accounted for differences among the populations in selection on traits such as corolla width and shape. Although not an example of coevolution, the results of this study predict that coevolutionary relationships should also have geographically variable outcomes when community structure differs. This is an important idea which has been developed over the last few decades by John Thompson and his colleagues (Thompson 1994, 2005).
Community composition has been shown to influence whether a relationship between an interacting species pair is mutualistic, commensalistic, or antagonistic (e.g., Thompson and Cunningham 2002). Similarly, in other pollination relationships, it can be imagined that the strength and even direction of selection exerted by one partner on the other would also be dependent on community context. For example, a community of long-tubed plants may select strongly for pollinators with long tongues. However, a community of mixed long- and short-tubed species may not select very strongly for long-tongued pollinators but may in fact select for pollinators with shorter tongues. As the pollinators evolve shorter tongues, they may then also select for shorter tubes in the long-tubed plant species. One outcome of this may be a landscape where tube and tongue lengths match each other closely in each population but where the magnitude of morphological traits differs between populations. This was first observed in oil-collecting bees and the flowers that they visit (Steiner and Whitehead 1990, 1991). Oil-collecting bees such as Rediviva neliana have long forelimbs which are used to mop up oil rewards from the twin spurs of the genus Diascia (Scrophulariaceae) and some orchids. When Steiner and Whitehead (1990) examined multiple populations of the bee and various Diascia species, they found a strong pattern of covariation between the average foreleg length of the bees and the spur length in Diascia populations.
Since then, even more spectacular examples of morphological covariation have been found in the tube and tongue lengths of long-tongued flies and the flowers that they visit (Anderson and Johnson 2008, 2009; Pauw et al. 2009). The tongues of these flies can be many times the length of their own bodies, and in the case of Moegistorynchus longirostris (Fig. 3) the tongues can reach a length exceeding 85 millimeters. In both of these systems, the tube and tongue lengths of interacting species show two- or three-fold variation across the landscape but were nevertheless closely correlated (Anderson and Johnson 2008, 2009; Pauw et al. 2009) (Figs. 4 and 5). These results have been interpreted as evidence to suggest that coevolution can generate geographic diversification in the morphology of interacting species pairs which may ultimately play an important role in the speciation process. Coevolution may also conceivably result in geographically divergent outcomes if abiotic factors, such as climate, determine how far the coevolutionary process is able to proceed.
The three pollination systems mentioned above were good candidate systems to study coevolution because the plants in all three species were dependent on a single pollinator species in each population, and the pollinators were all heavily dependent on these abundant plants as a source of food. Thus it can be imagined that the process of reciprocal selection operates. Although geographic covariation is consistent with the model of how tube–tongue length coevolution proceeds, demonstrating geographic covariation alone does not demonstrate that coevolution has occurred. This is because many other processes can also give rise to the geographic covariation of traits. If environmental factors have exactly the same effects on tube length and tongue length morphology, or even on other correlated body or floral traits, then tubes and tongues could correlate with each other without any reciprocal adaptation being involved in the process. Environmental variables and potentially correlated morphological traits (also see Steiner and Whitehead 1990, 1991) were incorporated into the models used to explain the geographic variation in the tongue lengths of the long-tongued fly Prosoeca ganglbaueri and its host plant Zaluzianskya microsiphon (Anderson and Johnson 2008). Despite the inclusion of these additional variables, tube length was best explained by the tongue lengths of the insect pollinators and vice versa, which supports the coevolution hypothesis. Furthermore, in one of these systems, the hypothesis of local co-adaptation was supported by reciprocal translocation experiments in which short-tubed plants translocated to sites with longer-tongued flies performed poorly relative to local forms with long tubes (Anderson and Johnson 2008, 2009).
Patterns of geographic trait covariation can also arise if one species adapts to another but not vice versa (i.e., unilateral evolution instead of coevolution). Perhaps the best documented case is the guild of long-proboscid fly-pollinated plants studied by Anderson et al. (2005) and Anderson and Johnson (2009). Anderson et al. (2005) demonstrated that the long-tongued fly P. ganglbaueri was the main pollinator of Z. microsiphon as well as the orchid Disa nivea. One difference between these two plants is that Z. microsiphon offers nectar rewards to its pollinators, but D. nivea offers no rewards. In a case of floral Batesian mimicry, D. nivea superficially resembles the rewarding plant Z. microsiphon and in so doing deceives pollinators into visiting it through mistaken identity. As a result, fly pollinators gain no benefit in matching the tube lengths of these rewardless orchids, but the orchid spurs nevertheless match the tongues of the flies as this maximizes the efficiency of pollen transfer (Fig. 5). Thus, although the orchids are not directly involved in a coevolutionary race with the flies, coevolution still affects them indirectly because they have to keep pace with the coevolutionary race between the flies and other rewarding plants, leading to identical patterns of geographic trait matching (Fig. 5).
Rewardless plants may not be the only plants tracking the evolutionary races of others. Entire guilds of less common plants may track coevolutionary races instead of driving them because they are too rare to exert much selective pressure on the pollinators. Anderson and Johnson (2009) and Pauw et al. (2009) found local convergence of floral morphology among unrelated plant species in the same community. Character traits such as tube length were more similar among different species in the same communities than they were between different populations of the same species. The important message from this is that trait evolution in coevolving species can have implications for other guild members that either track the evolution of these traits or become incorporated into these guilds. One of us recently argued that these pollination guilds can be interpreted as evolving niches which drive diversification (Johnson 2010).