Diversification through multitrait evolution in a coevolving interaction

Abstract

Mutualisms between species are interactions in which reciprocal exploitation results in outcomes that are mutually beneficial. This reciprocal exploitation is evident in the more than a thousand plant species that are pollinated exclusively by insects specialized to lay their eggs in the flowers they pollinate. By pollinating each flower in which she lays eggs, an insect guarantees that her larval offspring have developing seeds on which to feed, whereas the plant gains a specialized pollinator at the cost of some seeds. These mutualisms are often reciprocally obligate, potentially driving not only ongoing coadaptation but also diversification. The lack of known intermediate stages in most of these mutualisms, however, makes it difficult to understand whether these interactions could have begun to diversify even before they became reciprocally obligate. Experimental studies of the incompletely obligate interactions between woodland star (Lithophragma; Saxifragaceae) plants and their pollinating floral parasites in the moth genus Greya (Prodoxidae) show that, as these lineages have diversified, the moths and plants have evolved in ways that maintain effective oviposition and pollination. Experimental assessment of pollination in divergent species and quantitative evaluation of time-lapse photographic sequences of pollination viewed on surgically manipulated flowers show that various combinations of traits are possible for maintaining the mutualism. The results suggest that at least some forms of mutualism can persist and even diversify when the interaction is not reciprocally obligate.

Keywords: coevolution; correlated traits; geographic divergence; trait matching.

Fig. 1.

Divergence in morphology and the interaction between woodland star (Lithophragma spp.) species and their Greya moth pollinators. A window has been surgically cut into the side of each flower to show how pollination occurs during oviposition. As she punctures the floral ovary with her ovipositor, or slides through an opening in the side of the style to lay eggs, a moth simultaneously pollinates the flower with pollen adhering to her abdomen. Flowers vary among species from those having a completely inferior ovary, short style, and a stigma receptive only along the sides (Upper Left) to those having a completely superior ovary, a long style, and a stigma receptive over the upper stigmatic surface (Lower Right). For scale, length of a moth wing averages 6.6–7.7 mm among these populations, and floral width averages 3.0–4.0 mm. (Upper, Left to Right) Plants in the L. parviflorum clade: L. parviflorum North, L. parviflorum South, and L. affine. (Lower, Left to Right) Plants in the L. heterophyllum clade: L. bolanderi, L. cymbalaria, and L. heterophyllum. Moths are all members of the G. politella species complex.

Fig. 2.

Divergence in size and shape among Lithophragma plant populations (Left) and G. politella moth populations (Right) analyzed using principal component analysis. Values in parentheses after the axis labels are the percentage of variance attributable to that principal component axis. n = (plants; moths): L. parviflorum North (36; 200), L. parviflorum South (40; 20), L. affine (42; 48), L. heterophyllum (30; 12), L. cymbalaria (30; 48), L. bolanderi (30; 40).

Fig. 3.

Relative accuracy of fit of models to the observed data for geographic covariation of woodland star floral traits and Greya moth traits. The observed data are the pattern of geographic covariation in local plant traits compared with local moth traits (plant traits vs. moth traits). The alternative models include either random assignment of individuals to populations or random assignment of individuals only to populations within the larger clade from which they were drawn (e.g., assignment of L. bolanderi moths to plants within the L. heterophyllum, L. cymbalaria, and L. bolanderi clade). Models based on these assignments are called random, local, and structured. Accuracy is defined here as A = 1 − |(observed − expected)/observed|, in which observed = observed value, expected = mean value of a given model, and |x| is the absolute value of the number. The higher the value of A, the higher the accuracy, scaled to a maximum value of 1.

Fig. 4.

Distribution of the number of developing seeds after a single pollination/oviposition bout by a moth in the G. politella species complex. (Left) Three populations in the L. parviflorum clade. (Right) Three populations in the L. heterophyllum clade. Values are means ± 1 SE. n = 62 flowers for L. parviflorum N, 25 for L. parviflorum S, 25 for L. affine, 20 for L. heterophyllum, 45 for L. cymbalaria, and 28 for L. bolanderi.

Fig. 5.

Pollination efficacy of G. politella moths pollinating their local woodland star species compared with a woodland star species from a different locality. Values show a significant interaction effect of moth plant × plant population (Likelihood ratio χ²_1,99 = 6.01 P = 0.014, generalized linear model). Values are means ± 1 SE. Number of trials = 45 L. cymbalaria moths on L. cymbalaria plants; 11 L. cymbalaria moths on L. bolanderi plants; 28 L. bolanderi moths on L. bolanderi plants; 19 L. bolanderi moths on L. cymbalaria plants.