The ecology and evolution of seed predation by Darwin's finches on Tribulus cistoides on the Galápagos Islands

Abstract

Predator-prey interactions play a key role in the evolution of species traits through antagonistic coevolutionary arms races. The evolution of beak morphology in the Darwin's finches in response to competition for seed resources is a classic example of evolution by natural selection. The seeds of Tribulus cistoides are an important food source for the largest ground finch species (Geospiza fortis, G. magnirostris, and G. conirostris) in dry months, and the hard spiny morphology of the fruits is a potent agent of selection that drives contemporary evolutionary change in finch beak morphology. Although the effects of these interactions on finches are well known, how seed predation affects the ecology and evolution of the plants is poorly understood. Here we examine whether seed predation by Darwin's finches affects the ecology and evolution of T. cistoides. We ask whether the intensity of seed predation and the strength of natural selection by finches on fruit defense traits vary among populations, islands, years, or with varying finch community composition (i.e., the presence/absence of the largest beaked species, which feed on T. cistoides most easily). We then further test whether T. cistoides fruit defenses have diverged among islands in response to spatial variation in finch communities. We addressed these questions by examining seed predation by finches in 30 populations of T. cistoides over 3 yr. Our study reveals three key results. First, Darwin's finches strongly influence T. cistoides seed survival, whereby seed predation varies with differences in finch community composition among islands and in response to interannual fluctuations in precipitation. Second, finches impose phenotypic selection on T. cistoides fruit morphology, whereby smaller and harder fruits with longer or more spines exhibited higher seed survival. Variation in finch community composition and precipitation also explains variation in phenotypic selection on fruit defense traits. Third, variation in the number of spines on fruits among islands is consistent with divergent phenotypic selection imposed by variation in finch community composition among islands. These results suggest that Darwin's finches and T. cistoides are experiencing an ongoing coevolutionary arms race, and that the strength of this coevolution varies in space and time.

The role of spines in anthropogenic seed dispersal on the Galápagos Islands

“…The different functions of upper and lower spines are likely attributed to the fact that upper spines are typically oriented so they are pointing upwards, almost perpendicular to the ground, whereas the lower spines are often shorter and pointing outward in an orientation that likely makes it more difficult for them to adhere to surfaces (Figure , Figure ). These findings suggest that both seed predation and dispersal likely affect adaptive evolution of upper spines, whereas adaptive evolution of lower spines is solely affected by seed predators on the Galápagos (Carvajal‐Endara et al, ). It has already been demonstrated that the strength and direction of selection by seed predators varies across islands as a function of the finch community, and in response to variation in annual precipitation (Carvajal‐Endara et al, ).…”

“…These findings suggest that both seed predation and dispersal likely affect adaptive evolution of upper spines, whereas adaptive evolution of lower spines is solely affected by seed predators on the Galápagos (Carvajal‐Endara et al, ). It has already been demonstrated that the strength and direction of selection by seed predators varies across islands as a function of the finch community, and in response to variation in annual precipitation (Carvajal‐Endara et al, ). We do not know how seed dispersal varies among islands, but given that most islands are uninhabited by humans, and in light of the prominent role of anthropogenic seed dispersal on the Galápagos (see below), it is likely that selection on upper spines imposed by dispersal agents varies tremendously.…”

“…For example, many plants have hooks, barbs, and spines that adhere to animal fur, bird feathers, and feet (Sorensen, ). In the case of T. cistoides , a recent study showed that spines reduce seed predation by Darwin's finches on the Galápagos Islands (Carvajal‐Endara et al, ). Longer upper spines and the presence of lower spines reduced seed predation, and this was especially important on islands with large‐beaked finches and following dry years when seed sources were diminished.…”

“…Mericarps are very hard and difficult to open (Grant, ) and are typically protected by four spines, with one pair of spines on the upper dorsal surface and a second pair of spines on the lower dorsal surface of the mericarp (Figure a). Although most mericarps have four spines, Tribulus vary in spine number on the Galápagos, with some plants producing mericarps with only two spines in either the upper or lower dorsal position, and other plants producing mericarps that completely lack spines (Carvajal‐Endara et al, ; Grant, ; Figure ). Moreover, although all Tribulus spp.…”

“…A combination of recent experiments and natural history observations suggest that seed predators and dispersal may impose selection on spines. A recent study showed that spines act as an antipredator defence against three Darwin's finch species ( G. fortis , G. magnirostris , G. conirostris ), whereby upper and lower spines reduce seed predation (Carvajal‐Endara et al, ). However, this selection varied in space and time depending on climatic variation and the presence of large‐beaked finch species ( G. magnirostris and G. conirostris ).…”