The ecology and evolution of seed predation by Darwin’s finches on Tribulus cistoides on the Gal�apagos Islands

SOF�IA CARVAJAL-ENDARA ,1,10 ANDREW P. HENDRY ,1,2 NANCY C. EMERY ,3 COREY P. NEU ,4

DIEGO CARMONA ,5 KIYOKO M. GOTANDA ,6 T. JONATHAN DAVIES ,1,7 JAIME A. CHAVES ,8 AND MARC T. J. JOHNSON 9

1Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montr�eal, Quebec H3A 1B1 Canada 2Redpath Museum, McGill University, 859 Sherbrooke Street West, Montr�eal, Quebec H3A 0C4 Canada

3Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, Colorado 80309-0334 USA 4Department of Mechanical Engineering, University of Colorado Boulder, Boulder, Colorado 80309-0427 USA

5Departamento de Ecolog�ıa Tropical, Campus de Ciencias Biol�ogicas y Agropecuarias, Universidad Aut�onoma de Yucat�an, M�erida, Yucat�an M�exico

6Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ United Kingdom 7Biodiversity Research Centre, Departments of Botany, Forest and Conservation Sciences, University of British Columbia, 2212 Main

Mall, Vancouver, British Columbia V6T 1Z4 Canada 8Colegio de Ciencias Biol�ogicas y Ambientales – Extensi�on Gal�apagos, Universidad San Francisco de Quito, Campus Cumbay�a, Casilla

Postal 17-1200-841, Quito, Ecuador 9Department of Biology, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6 Canada

Citation: Carvajal-Endara, S., A. P. Hendry, N. C. Emery, C. P. Neu, D. Carmona, K. M. Gotanda, T. J. Davies, J. A. Chaves, and M. T. J. Johnson. 2020. The ecology and evolution of seed predation by Darwin’s finches on Tribulus cistoides on the Gal�apagos Islands. Ecological Monographs 90(1):e01392. 10. 1002/ecm.1392

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 evolu- tion 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 inten- sity 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 examin- ing 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.

Key words: adaptive divergence; coevolutionary arms race; geographic mosaic; phenotypic selection; plant defense; trophic interactions.

INTRODUCTION

Antagonistic interactions play a major role in the evo- lutionary diversification of traits that mediate species interactions (Thompson 1999, Vamosi 2005, Paterson

Manuscript received 20 December 2018; revised 8 May 2019; accepted 9 July 2019. Corresponding Editor: Todd M. Palmer

10 E-mail: [email protected]

Article e01392; page 1

Ecological Monographs, 90(1), 2020, e01392 © 2019 by the Ecological Society of America

 

 

et al. 2010). Plant–herbivore interactions have long been used as a model to understand the evolution and ecology of antagonistic interactions (Ehrlich and Raven 1964, Fritz and Simms 1992, Agrawal 2011). Plants employ a wide diversity of mechanical and chemical defense strategies to avoid the negative effects of herbivores, including seed predators (Crawley 1983, Carmona et al. 2011). In turn, herbivores and predators use a variety of strategies to counteract plant defenses, including behav- ioral, morphological, and physiological offensive traits (Karban and Agrawal 2002). Selection that favors traits that better protect plants against herbivores and preda- tors can lead to contemporary evolutionary changes in plant defense traits (Agrawal et al. 2012, Z€ust et al. 2012, Didiano et al. 2014). Here, we study the effect of seed predation by Darwin’s finches on plant ecology, and its potential role in the evolution of seed defense traits by natural selection. The interaction between Darwin’s finches and their food

plants on the Gal�apagos Islands is a famous andwell-studied example of contemporary evolution (Grant and Grant 2014). Previous studies in agroup of Darwin’s finches known as ground finches show that evolutionary changes in beak size and shape are driven by the availability and distribution of seeds (Lack 1947, Grant 1986, Grant and Grant 1995). Ground finches are primarily seed predators and poor seed dispersers; they usually crush the seeds before ingesting them, and their feces and gut samples rarely contain viable seeds (Buddenhagen and Jewell 2006, Guerrero and Tye 2009). In general, ground finches are opportunistic feeders that eat a large variety of seed species, but when resources are limited following droughts, finches become dependent on the seeds of a smaller number of plant species that are often harder and more difficult to open (Grant and Grant 1995, De Le�on et al. 2014). The ability to exploit those seeds is largely influ- enced by beak size and shape (Lack 1947, Grant and Grant 1995, De Le�on et al. 2011). Because seeds are a major part of their diet, and because ground finches exhibit preferences for certain seeds, it is anticipated that finches have an important effect on the ecology and evolution of plants on the Gal�apagos Islands. However, despite the well-developed liter- ature on the interactions between Darwin’s finches and plants (Boag and Grant 1981, Schluter and Grant 1984, Price 1987, Grant and Grant 1999, De Le�on et al. 2014), the eco- logical and evolutionary consequences of seed predation by finches on plants remains largely unexplored. The effects of seed predation by finches on plants on

the Gal�apagos Islands are expected to be mediated by both climate and the strength of species interactions. Pre- dation pressure by finches on seeds during periods with high precipitation might be negligible owing to the high production of seeds, and the increased availability of other food resources such as insects (Grant and Boag 1980, Boag and Grant 1984, Price 1985, Gibbs and Grant 1987). However, during extended droughts, when seed production is reduced, selective seed predation by finches (Grant 1986, De Le�on et al. 2014, Grant and Grant 2014) could greatly influence seed survival, plant

distributions, and the evolution of seed defense traits. Selection imposed by finches on seed defense traits is expected to play the most important role for plant species that are commonly exploited by finches. Caltrop (Tribulus cistoides) is one of the main food sources for some species of ground finches during dry periods, and it is credited with driving the evolution of beak morphology in the Medium Ground Finch (Geospiza fortis) during periods of drought (Grant and Grant 2006, 2014). The fruits of T. cistoides possess morphological features thought to provide defenses against predation, including multiple long spines and a hard protective tissue (Grant 1981; Fig. 1). Grant (1981) showed that, within a T. cistoides population on Daphne Major island, fruits with two spines were eaten more frequently than fruits with four spines, suggesting that finches impose selection on T. cis- toides fruit morphology. However, selection on T. cis- toides fruits has not been assessed across years or in populations on other islands, and the association between fruit morphology and seed survival in response to finch predation across the archipelago remains unclear. An additional factor that might influence the effects of

seed predation by finches on plants on the Gal�apagos Islands is variation in the composition of finch communi- ties. Ground finches are broadly distributed within the archipelago and most of the islands harbor several species that differ in beak size and shape. Among ground finches, only the Large Ground Finch (G. magnirostris), the Large Cactus Finch (G. conirostris), and the Medium Ground Finch (G. fortis) are able to exploit T. cistoides seeds (Grant 1981, Grant and Grant 1982). These species, however, are not uniformly distributed across the islands. The contempo- rary faunas of some major islands have one of the large- beaked G. magnirostris and G. conirostris species and the small-beaked G. fortis, such as Santa Cruz and Isabela (Fig. 2), whereas others lack the large-beaked species, such as Floreana and San Crist�obal. This spatial variation in the finch community could have large ecological and evolution- ary consequences because G. magnirostris are superior at feeding on T. cistoides seeds relative to G. fortis (Grant 1981), which could lead to divergent patterns of predation and selection imposed on fruit morphology across the Gal�apagos Islands. Our study focuses on understanding the effects of seed

predation by Darwin’s finches on the ecology and evolu- tion of T. cistoides. We asked the following three ques- tions: (1) Does seed predation by finches vary among populations, islands, finch community composition, and years? We expected seed predation to vary among years; due to variation in annual precipitation, and also in asso- ciation with finch community composition (small-beaked finches are expected to eat fewer seeds of T. cistoides dur- ing wetter conditions). (2) Do finches impose selection on T. cistoides fruit morphology, and does selection vary among populations, islands, years, and with finch com- munity composition? We expected the strength of selec- tion on fruit morphology to vary over time in correspondence with precipitation, and spatially among

Article e01392; page 2 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

islands in association with finch community composition: large-beaked finch species eat seeds more readily and likely impose differing selection on fruit morphology compared to communities with only small-beaked

finches. (3) Does T. cistoides fruit morphology differ among islands with contrasting finch community compo- sition (i.e., the presence/absence of large-beaked finches)? We expected spatial variation in fruit morphology to

FIG. 1. (a) Tribulus cistoides fruits (schizocarps), from left to right: a green immature fruit, a mature dry fruit, and a fruit attached to a maternal plant. (b) Two sets of dry mericarps, corresponding to two fruits of different plants, showing variation in size and number of spines. Mericarps in the upper set are larger and have four spines while mericarps in the lower set are smaller and have only two spines. (c) Opened mericarp to expose seed compartments, one empty compartment and three compartments with seeds inside. (d) Geospiza fortis (Medium Ground Finch) holding a T. cistoides mericarp. Mericarps showing marks observed (e) when seeds are eaten by finches, (f) when seeds are eaten by insects, and (g) when seeds germinate. Photo credits: Marc T. J. John- son (a [left and middle], c, and f), Andrew P. Hendry (b), Kiyoko M. Gotanda (d and e), and Sof�ıa Carvajal-Endara (a [right] and g).

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 3

 

 

reflect spatial variation in finch community composition, which would be consistent with adaptive responses to divergent selective pressure. To address these questions, we examined variation in T. cistoides fruit morphology and patterns of seed predation in 30 natural populations across seven islands of the Gal�apagos archipelago over 3 yr, and performed a seed predation experiment in a popu- lation on one of the islands. Our study is one of the first to address the potential effect of seed predation by Dar- win’s finches on the evolution of Gal�apagos plants. We consider the importance of these results for understand- ing the potential coevolutionary interactions between Darwin’s finches and the plants whose seeds they con- sume.

METHODS

Study site and system

The Gal�apagos archipelago is located in the Pacific Ocean approximately 1,000 km west of the Ecuadorian coast in South America, and it comprises 14 major

islands and many small islets (Geist 1996). We restricted our study to seven islands that vary in finch community composition (Fig. 2), and that harbor at least one of the three finch species that consume T. cistoides seeds: G. fortis, G. conirostris, and G. magnirostris. The diet of these three finch species varies according to the size and shape of their beaks, as well as the spatial and temporal availability of seeds (Schluter and Grant 1984; Grant and Grant 1999, De Le�on et al. 2014). During dry peri- ods, especially the droughts that accompany La Ni~na events, preferred foods are limited and, hence, T. cis- toides seeds become a main food source for these finch species (Grant and Grant 2014). Tribulus cistoides (Zygophyllaceae) is a perennial pros-

trate herb native to subtropical and tropical Africa and now is widespread in tropical and subtropical arid coastal habitats around the world (Porter 1972). Broadly distributed across the Gal�apagos archipelago, it is usu- ally found in arid lowlands and coastal regions, where it grows in discrete patches close to roads, trails, and shorelines (Porter 1971). Tribulus cistoides plants can flower at any time of year on the Gal�apagos Islands, but most of its vegetative growth occurs during the wet sea- son (from January to May), they produce fruits called schizocarps (Fig. 1a), which contain five individual seg- ments referred to as mericarps that typically separate from one another as the fruit dries (Fig. 1b) (Wiggins and Porter 1971). Each T. cistoides mericarp is a hard fibrous structure that includes from one to seven seeds contained within individual compartments (Fig. 1c). Mericarps typically have four spines (two upper and two lower sharp protuberances), but the size and position of spines varies greatly among individual plants, and some mericarps completely lack some or all spines (Fig. 1b). The spiny mericarps are also a means of seed dispersal (Porter 1972); fruits adhere easily to animals, such as the feet of seabirds (Wiggins and Porter 1971). Ocean cur- rents and humans are considered important vectors of long-distance dispersal, whereby fruits travel long dis- tances by getting attached to shoes and rubber tires (Holm et al. 1977). To extract the seeds, finches pick up mericarps from

the ground after they have dropped from the plant. The finches often hold the mericarp laterally between their mandibles, and apply pressure by closing their beak, moving the upper and lower mandibles sideways to each other, to crack the mericarp wall, sometimes stabilizing the mericarp against a rock or the ground (Fig. 1d, see Video S1). The mericarps are very durable and long lived and this, combined with the very distinct damage left by finch predation, makes it possible to determine which mericarps have been depredated even months after a pre- dation event. Specifically, finches remove the ventral sur- face of the hard mericarp tissue protecting the seeds, exposing the empty seed compartments from which seeds are removed (Fig. 1c), often one compartment at a time (Video S1) (Grant 1981). Mericarps depredated by finches (Fig. 1e) are easily distinguished from mericarps

FIG. 2. Map showing the seven islands of the Gal�apagos archipelago where Tribulus cistoides fruits were sampled. Black and blue identify the islands where large-beaked ground finches are present: the Large Ground Finch (Geospiza magnirostris) is present on Isabela and Santa Cruz and the Large Cactus Finch (G. conirostris) is found on Espa~nola. Orange identifies the islands where these large-beaked finches are absent. The Med- ium Ground Finch (G. fortis) is present in all visited islands except in Espa~nola.

Article e01392; page 4 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

consumed by insects, which make smaller circular “drill” holes (Fig. 1f), and from mericarps from which seeds have germinated, which are apparent as empty seed com- partments are still partially enclosed by the mericarp wall (Fig. 1g), without the rough damage characteristic of seed predation by finches (Fig. 1e). Other than finches and insects, no other common predators of T. cistoides seeds are found on the Gal�apagos Islands. Unopened mericarps of T. cistoides were found in the gizzard contents of a Gal�apagos dove (Zenaida galapa- goensis); however, T. cistoides fruits are not a typical part of the diet of this species (Grant and Grant 1979).

Population sampling and experimental design

To explore impacts of seed predation by finches, we sampled nearly 7,000 mericarps from 30 T. cistoides populations across seven islands of the archipelago over 3 yr (2015–2017). Considering only ground finch species that consume T. cistoides seeds, finch seed-predator communities on three of the selected islands (Santa Cruz, Isabela, and Espa~nola) include large-beaked finch species (G. magnirostris or G. conirostris), whereas finch communities on the other four islands (San Crist�obal, Floreana, Baltra, and Seymour Norte) lack large-beaked finch species (Fig. 2). The medium-beaked species, G. fortis, is present on all sampled islands except Espa~nola (Fig. 2). Sampling was performed between the months of February and March, corresponding to the end of the dry season and beginning of the wet season (Fig. 3a), which is when the finches’ preferred food is expected to be most scarce and their consumption of T. cistoides seeds becomes highest. On four of the islands (Santa Cruz, Isabela, San Crist�obal, and Floreana), we repeated sampling annually from 2015 to 2017. During this period, the archipelago experienced strong climatic variation, including an El Ni~no event that occurred in 2015 (Stramma et al. 2016) and resulted in higher pre- cipitation relative to the preceding and subsequent years (Fig. 3b). The number of T. cistoides populations sampled var-

ied among islands (one to eight populations) due to spa- tial variation in the abundance of plants, with a “population” considered to be a discrete patch of T. cis- toides plants separated by at least 500 m from any other patch. Information about the populations sampled each year (island, geographic coordinates) is provided in Appendix S1: Table S1. From each population, we col- lected approximately 100 mericarps chosen haphazardly across the area; we made every effort to select mericarps “blindly” to avoid biases, so that mericarps represented a random subset of the morphological traits present in the population as much as possible. Most mericarps are expected to be from the previous season, but it is possi- ble that some mericarps were >1 yr old. A total of 6,391 mericarps were collected across all islands, populations, and years. For each mericarp, we used digital calipers to measure mericarp length (mm), width (mm), and the

distance between the tips of the upper spines (upper spine size, mm) located toward the distal end of the mericarp, and we noted the presence or absence of lower spines and the number of seeds removed by finches (Fig. 4a). To estimate the total number of seeds origi- nally produced in each mericarp we opened and counted the number of seeds in 752 mericarps, collected from five populations on Santa Cruz island in 2015. We evaluated the relationship between the number of seeds per meri- carp and mericarp morphology by fitting the following allometric equation: number of seeds = log(length) + log(width) + log(length) 9 log(width). We then used this model to predict the total number of seeds per mericarp (R2 = 0.48). To test whether there was variation in fruit morphol-

ogy among individual plants for selection to act upon, we sampled mericarps from two T. cistoides populations (AB and EG) on Santa Cruz island during February 2015 (see geographic information in Appendix S1: Table S1). From each population, we sampled 15 indi- vidual plants, from each of which we collected four com- plete (i.e., uneaten) and mature fruits (schizocarps), with each schizocarp having four to five mericarps. In total,

FIG. 3. Variation in (a) monthly and (b) annual precipita- tion (mm) from 2014 to 2017 on Santa Cruz island. Precipita- tion data were obtained from a meteorological station at the Charles Darwin Research Station (CDRS).

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 5

 

 

we sampled 583 mericarps for measurement of morpho- logical traits including length, width, upper spine size, presence/absence of lower spines, and mericarp mass (to the nearest milligram using a digital balance GEM20; Smart Weigh, Jintan, China). To experimentally test whether finches impose selec-

tion on mericarp morphology, we performed a seed pre- dation experiment during March 2016. First, we collected 600 mature and intact mericarps from a T. cis- toides population (EG) located on Santa Cruz island (see geographic information in Appendix S1: Table S1). We measured four traits from each mericarp (length, width, upper spine size, and presence/absence of lower spines), and gave each mericarp a unique mark with indelible ink so mericarps could be individually identi- fied. We also applied an experimental removal of spines from a haphazard subset of the 400 mericarps by clipping either one or both of the upper spines, which allowed us to experimentally test the functional role of spines in defense. The marked mericarps were then exposed to natural finch predation on 40 circular plastic trays (~15 cm in diameter). The trays were placed across the area where the mericarps were collected, at least 30 cm apart from each other, and were monitored every three days. The mericarps were recovered after 30 d. Finally, to evaluate the relationship between mericarp

morphology and hardness, we used 102 mericarps col- lected in 2017 from three populations on Isabela island and seven populations on Santa Cruz island (Appendix S1: Table S1). For each mericarp, we mea- sured hardness (0–100 value on a Shore D scale; Pam- push et al. 2011) using a handheld durometer (Asker, Super Ex, Type D, Kyoto, Japan). As the structure of the mericarp wall varies over its surface (Fig. 4b), we mea- sured hardness at six locations on each mericarp (see detailed information in Appendix S2: Fig. S1). In addi- tion, on each mericarp, we measured six morphological traits (length, width, depth, upper spine size, longest spine length, and spine position; Fig. 4a).

Statistical analyses

All statistical analyses were performed using R v. 3.4.2 (R Development Core Team 2008).

Does seed predation by finches vary among populations, islands, finch community composition, or years?—We used logistic linear mixed-effects models with the func- tion glmer in lme4 v. 1.1-14 package (Bates et al. 2015) to model the proportion of seed predation per popula- tion (proportion of mericarps with one or more seeds removed by finches). This model was fit as follows: pre- dation per population = year + finch community com- position + year 9 finch community composition + island + error. Year, finch community composition, and their interaction were treated as fixed effects, whereas island was included as a random effect. Finch commu- nity composition was categorized as 0 on islands where large-beaked finch species (G. magnirostris and G. conirostris) were absent (Floreana, San Crist�obal, Baltra, and Seymour Norte), and 1 on islands where large-beaked finch species were present (Isabela, Santa Cruz, and Espa~nola). To examine the association of pre- cipitation with seed predation during our study, we fit a similar model in which we replaced the fixed factor year with the total annual precipitation (mm) registered dur- ing the year that preceded each sampling. Precipitation measurements, obtained from a meteorological station placed on Santa Cruz island at the Charles Darwin Research Station (0°44037.600 S, 90°50021.900 W), were log10-transformed. We also fit the following model where the response variable was the proportion of seeds removed per mericarp, and mericarp was the unit of replication: proportion of seeds removed = year + finch community composition + year 9 finch community composition + island + popu- lation(island) + error. In this analysis, the proportion of seeds consumed per mericarp was calculated as the ratio between the number of seeds removed from the mericarp

FIG. 4. (a) Mericarp traits and morphological measurements. (b) Micro-computed tomography (lCT) image showing mericarp wall variation over its surface.

Article e01392; page 6 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

and the number of seeds predicted based on the traits of the mericarp. We included year and finch community composition as fixed effects, whereas island and popula- tion were included as nested random effects, with the parentheses denoting nested factors. Significance of fixed effects was assessed using a type II Wald’s chi-squared test, and the significance of random effects was assessed with likelihood-ratio tests. P values were divided by two because tests of the significance of random effects are one-tailed given that variance > 0 (Littell et al. 1996). Finally, to evaluate more directly the effect of the finch community on seed predation per year (at the level of population and mericarps), we fit the logistic mixed- effects models separately for each year. We performed the analyses described above including all islands and exclud- ing data from the three islands that were sampled only in 2016 (Espa~nola, Baltra, and Seymour Norte).

Do finches impose selection on T. cistoides fruit morphol- ogy and does selection vary among populations, islands, years, or with finch community composition?—We first confirmed that most mericarp traits examined (length, upper spine size, presence/absence of lower spines, and mass) exhibit substantial variation among individual plants, with the exception of mericarp width (Appendix S3: Table S1). Next, we measured phenotypic selection (sensu Lande and Arnold 1983) on mericarps sampled from natural populations using logistic mixed- effects models in the R package lme4 v. 1.1-14 (Bates et al. 2015) to examine the relationship between T. cis- toides fitness (seed survival) and fruit morphology (Jan- zen and Stern 1998). Estimates of T. cistoides seed survival included two variables: (1) a binary response, where 0 corresponded to a mericarp that had at least one seed removed and 1 to a mericarp that had no seeds removed, and (2) the proportion of seeds that survived finch predation per mericarp, calculated based on the estimated number of seeds per mericarp. Each of these response variables was considered in separate models, with mericarp traits treated as fixed effects. Mericarp length, width, and upper spine size were

log10-transformed to improve normality and standard- ized to a mean of 0 and a standard deviation of 1. Because of the correlation between mericarp width and length (r = 0.43), as well as a correlation between length and upper spine size (r = 0.51), we also performed a principal component analysis to obtain a principal com- ponent axis (PC1Size) that captures covariation among these traits. We also included mericarp lower spines as a binary response variable, with 1 indicating the presence of a lower spine and 0 the absence of the trait. In addi- tion, to test if selection on mericarp traits depended on year and finch community, we added the interaction between mericarp traits and these two factors, with island and population nested within island as random effects. To enable comparisons among years, we excluded the data from the three islands that were sam- pled only in 2016 (Espa~nola, Baltra, and Seymour

Norte) from this analysis. The full model was seed sur- vival = PC1Size + upper spine size + presence of lower spines + year + finch community + year 9 PC1Size + year 9 upper spine size + year 9 presence of lower spines + finch community 9 PC1Size + finch commu- nity 9 upper spine size + finch community 9 presence of lower spines + island + population(island) + island 9 PC1Size + island 9 upper spine size + island 9 presence of lower spine + error. To avoid overparameterization of the models, reduced

statistical power, and elevated type II error, we used the dredge function in the R package MuMIn v. 1.15. 6. (Bar- ton 2016) and glmer to compare the models resulting from all combinations of the fixed effects. This multi- model averaging approach provides the most comprehen- sive and powerful approach for finding the best-fitting models based on the lowest Akaike information criterion (AIC) values. The importance of each effect was evalu- ated from the best-fitting model selected for each response variable, with significance estimated using type II Wald’s tests in the case of fixed effects, and likelihood- ratio tests in the case of random effects as described above. We averaged the subset of models with AIC val- ues < 2 to estimate average coefficients for each indepen- dent variable using the function model.avg. To explore whether finches imposed selection on meri-

carps in the seed predation experiment, we also used logistic mixed-effects models in which seed survival was coded as 0 when the recovered mericarp had one or more seeds removed, and 1 when the mericarp had no seeds removed. This model had mericarp as the unit of replication and took the following form: Seed sur- vival = spine treatment + lower spines + PC1Size + tray. Spine treatment (a categorical variable coded as 0, 1, or 2 according to the number of large spines remaining on the mericarp), presence/absence of lower spines, and PC1Size (i.e., mericarp size) were included as fixed effects, and tray was included as a random effect. The signifi- cance of each fixed effect was evaluated using a type II Wald’s test. To evaluate the relationship between mericarp mor-

phology and mericarp hardness, we first ran three inde- pendent principal component analyses to collapse the hardness measures and morphological measures into separate, multivariate axes: PC1Global hardness included hardness measures from all six positions on the meri- carp, whereas PC1Local hardness included hardness mea- sures from the three hardest positions on the mericarp (Appendix S2: Table S1) that we expect to be most directly involved in protecting seeds from finches preda- tion. In this analysis, PC1Size was the first principal com- ponent generated from all six mericarp morphological traits (length, width, depth, upper spine size, longest spine, and spine position). We used a mixed-effects model to evaluate the relationship between hardness and morphology: PC1Global hardness = PC1Size + island + population(island), with PC1Size as fixed effect, and island and population nested within island treated

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 7

 

 

as random effects. We repeated this model using PC1Local hardness as the response variable. Two additional models were fit, replacing PC1Size with the six individual morphological variables in the same model to simultaneously evaluate the independent contributions of each morphological trait variable to variation in PC1Global hardness and PC1Local hardness. In each case, a model-averaging procedure was used. All data were standardized within populations to a mean of zero and standard deviation of one prior to analysis. R2 values were computed for mixed-effect models using the func- tion r.squaredGLMM from the R package MuMIn v. 1.15. 6 (Barton 2016); we estimated R2 values associated with fixed effects (R2 marginal), and R2 values associ- ated with fixed and random effects (R2 conditional).

Does T. cistoides fruit morphology differ among islands with contrasting finch community composition?—To evalu- ate if finch community composition (i.e., presence/ab- sence of large-beaked finches) influences T. cistoides fruit morphology, we first fit a linear mixed-effects model for each of the following traits: width, length, upper spines size, and the PC1size separately, using the lmer function from the lme4 v. 1.1-14 package (Bates et al. 2015). The data were fit to the following model: trait = finch community composition + year + finch community composition 9 year + island + population (island) + error, whereby parentheses indicate nested terms. Finch community composition, year, and the interaction between these factors were included as fixed effects, while island and population nested within island were modelled as random effects. The models were also fit for each year separately to test the effect of finch com- munity on mericarp traits in each year. Last, we ana- lyzed presence/absence of lower spines as a response variable; for this analysis, we fit a logistic mixed-effects model using the function glmer implemented in the lme4 v. 1.1-14 package (Bates et al. 2015).

RESULTS

Variation in seed predation by Darwin’s finches

Seed predation by finches varied among populations, islands, and years, as well as with finch community com- position. The proportion of seed predation per population differed among years (v2 = 208.60, P < 0.01) and islands (v2 = 74.00, P < 0.01). In 2016, a year following high pre- cipitation, we found 39% less predation than in 2015 and 45% less predation than in 2017. In addition, higher annual precipitation, registered on Santa Cruz island, was associated with reduced seed predation the following year (v2 = 203.45, P < 0.01). Among islands, mericarps on Isa- bela had 29% less predation than Santa Cruz and Flore- ana, and 39% less predation than San Crist�obal. The effect of finch community composition on the proportion of seed predation varied among years (finch commu- nity 9 year: v2 = 40.34, P < 0.01, Table 1 and Fig. 5).

Finch community composition did not influence the pro- portion of predation in 2015 (Z = �1.20, P = 0.23) or 2017 (Z = �1.40, P = 0.16). In contrast, in 2016, T. cis- toides experienced 32% higher predation on islands where the large-beaked finches are present (Z = 3.32, P < 0.01), compared to islands where they are absent. These results excluded data from the three islands that were sampled only in 2016 (Espa~nola, Baltra, and Sey- mour Norte); yet similar results were obtained when all islands were included (Appendix S4: Table S1). The pro- portion of seeds eaten per mericarp also showed varia- tion among years (v2 = 158.60, P < 0.001), and finch community composition (v2 = 7.14, P = 0.008; see Appendix S4: Table S2, Fig. S1). No effect of finch com- munity composition was seen for the proportion of seeds eaten per mericarp in 2016 (Z = 0.10, P = 0.809). How- ever, in 2015 and 2017, the proportion of seeds eaten per mericarp was 37% and 36% (respectively) lower on islands where the large-beaked finches were present com- pared to islands where they are absent. Overall, we found that, on islands where large-beaked finches were absent, predation rate per population decreased in the year fol- lowing high precipitation, and the proportion of seeds eaten per mericarp increased in drier years.

Phenotypic selection on T. cistoides fruit morphology

Finches imposed phenotypic selection on mericarp mor- phology (Table 2). In samples from natural populations, smaller mericarps (PC1Size: v

2 = 21.47, P < 0.001) with longer upper spines (v2 = 81.20, P < 0.001) were more likely to escape predation by finches. The presence of lower spines also reduced predation, but the effect was marginally nonsignificant (v2 = 3.36, P = 0.067). The pat- tern of selection on upper spine size and on the presence of lower spines depended on finch community composi- tion (finch community 9 upper spine size, v2 = 9.72, P < 0.002; finch community 9 lower spines, v2 = 6.25, P = 0.012; Table 2). Longer upper spines and the presence of lower spines tended to provide greater protection to mericarps against seed predation on islands where large- beaked finch species were absent (Fig. 6a). Selection on mericarp upper spine size and the pres-

ence of lower spines also varied among years (year 9 upper spine size, v2 = 11.56, P = 0.003; year 9 lower spines, v2 = 9.83, P = 0.007). Selection for longer upper spines was stronger in 2016 (Fig. 6b) than in 2015 and 2017, whereas selection on the presence of lower spines was strongest in 2015. Model-averaged coefficients are presented in Appendix S5: Table S1. Sim- ilar results were obtained when the proportion of seeds that survived predation per mericarp was used as the response variable (Appendix S5: Table S2), except that we found stronger evidence for selection on the presence of lower spines (v2 = 23.11, P < 0.001) and selection on mericarp traits did not vary between years (P > 0.5). In our short-term seed predation experiment in 2016,

we recovered 32 of the 40 trays containing mericarps.

Article e01392; page 8 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

From these trays, 18.3% of the mericarps showed evi- dence of predation by finches, 69.2% were uneaten, and 12.5% were not recovered. In our analysis, we included only the mericarps that were recovered. No relationship was found between number of upper spines and survival to finch predation (v2 = 1.26, P = 0.533), but larger mericarps were more likely to escape predation (PC1Size, v2 = 5.09, P = 0.024), contrasting with the patterns we observed in natural populations.

Relationship between variation of fruit morphology and hardness

Morphological variation in mericarps was associated with variation in mericarp hardness. Mericarp hardness varied substantially among locations on the surface of mericarps (F5, 235 = 15.301, P < 0.001; Appendix S2: Table S2). We detected a negative relationship between overall mericarp hardness (PC1Global hardness) and overall mericarp size (PC1Size; b = �0.437 � 0.102, v2 = 16.876, P < 0.001, R2conditional = 0.397, R

2 marginal= 0.147, N = 102;

Fig. 7). We detected a similar negative relationship when only the hardest locations on the mericarp (PC1Local hardness) were evaluated (b

length = �0.239 � 0.107, P = 0.02;

bwidth = �0.404 � 0.090, P < 0.0001, R2conditional = 0.335, R2marginal = 0.231, N = 102; Fig. 7). When we replaced PC1size with the six individual morphological variables, the best model identified a negative relation- ship between mericarp length and width and PC1Global hardness (blength = �0.300 � 0.096, P = 0.002; bwidth = �0.435 � 0.084, P < 0.0001; R2conditional = 0.458, R2marginal = 0.334; Fig. 7). Collectively, these analyses show that smaller T. cistoides mericarps tend to be harder than larger mericarps.

Effect of finch community composition on fruit morphology

Mericarp morphology varied substantially among populations, islands, and years (Fig. 8; Appendix S6: Table S1). We found differences among islands in meri- carp length (v2 = 11.9, P < 0.01) and upper spine size (v2 = 5.08, P < 0.02). For instance, mericarps from Isa- bela were shorter and had shorter upper spines than did mericarps from the other islands. Finch community composition was associated with the presence/absence of lower spines in mericarps (v2 = 17.98, P < 0.01). The presence of the large-beaked finch species was associated

TABLE 1. Logistic mixed-effects models analyzing variation in the proportion of mericarps experiencing seed predation per population among islands and years.

Factor Estimate Z v2 P

a Fixed effects Finch community 2.85 0.09 Year 208.60 <0.001 Finch community 9 Year 40.34 <0.001

Random effect Island 74.00 <0.001

b Year 2015 Fixed effect

Finch community �0.71 (0.59) �1.20 0.23 Random effect

Island 125.97 <0.001 Year 2016 Fixed effect

Finch community 0.39 (0.12) 3.32 <0.01 Random effect

Island 0.00 0.50 Year 2017 Fixed effect

Finch community �0.47 (0.34) �1.40 0.16 Random effect

Island 32.36 <0.001

Notes: The response variable was the proportion of mericarps that had at least one seed removed by finches in each population sample (N = 100 in most populations). Finch community composition was considered as a fixed binary factor, with 0 indicating the absence of the large-beaked finch species Geospiza magnirostris (only G. fortis present) and 1 indicating its presence. Estimate is a mean with SE in parentheses. In part a, the model included year, finch community composition, and the interaction between those factors as fixed effects. The effect of island was included as a random effect. In part b, separate models were fit for each year. The v2

and P values of fixed factors were estimated using type II Wald tests and random effects were estimated using likelihood-ratio tests with one degree of freedom. Effects significant at P < 0.05 are shown in boldface type. These models only include data from islands sampled in multiple years (see models including all islands in Appendix S4: Table S1).

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 9

 

 

with 67% more mericarps having lower spines. However, finch community composition was not associated with differences in mericarp width (v2 = 0.10, P = 0.75), length (v2 = 0.24, P = 0.62), or upper spine size (v2 = 0.0, P = 0.44). The effect of finch community composition on fruit morphology also varied among years (mericarp width, v2 = 16.56, P < 0.01; length, v2 = 41.60, P = 0.03; upper spine size, v2 = 53.90, P < 0.01; and lower spines, v2 = 47.03, P < 0.01). When we examined the effect in each year, we found a signifi- cant effect of finch community composition on the pres- ence of lower spines in 2017 (v2 = 11.13, P < 0.01), but no effect of finch community composition on the other traits (mericarp width, length, and upper spine size). Divergence patterns of PC1size were similar to those observed for mericarp width and length (see Appendix S6: Table S1).

DISCUSSION

Seed predation by Darwin’s finches was found to influence ecological and evolutionary processes associ- ated with T. cistoides. Several findings address our ini- tial questions. First, Darwin’s finches were an important source of mortality for T. cistoides seeds, with the inten- sity of seed predation varying over time and space in partial association with finch community composition. Second, finches imposed phenotypic selection on T. cis- toides fruit traits whereby seeds within smaller and

FIG. 5. Variation in the proportion of seed predation per population among islands, years, and with contrasting finch commu- nity composition (represented by different colors). The data correspond to the populations sampled on the four islands (represented by different shapes) that were visited repeatedly over three years of the study (2015–2017). The mean (dark circles) and the standard error (dark bar) of the proportion of mericarps with one or more seeds removed by finches in populations sampled from islands where the large-beaked finch species are absent (0), and present (1).

TABLE 2. Generalized mixed-effects model analyzing pheno- typic selection on mericarp traits by finches.

Factor v2 P

Fixed effects Finch community 1.44 0.229 Year 188.70 <0.001 PC1(Size) 21.47 <0.001 Upper spine size 81.20 <0.001 Lower spines 3.36 0.067 Finch community 9 Upper spine size 9.72 0.002 Finch community 9 Lower Spines 6.25 0.012 Finch community 9 Year 45.46 <0.001 Year 9 PC1(Size) 3.65 0.161 Year 9 Upper spine size 11.56 0.003 Year 9 Lower spines 9.83 0.007

Random effect Island 0.00 0.500 Population 462.80 <0.001 Island 9 PC1(Size) 0.00 0.500 Island 9 Upper spine size 0.00 0.500 Island 9 Lower spines 5.14 0.012

Notes: The response variable seed survival is binary, with 0 indicating mericarps with one or more seed removed by finches and 1 indicating complete mericarps with no seeds removed. Finch community composition was considered as a fixed binary factor, with 0 indicating the absence of the large-beaked finch species Geospiza magnirostris (only G. fortis present) and 1 indi- cating its presence. The v2 and P values of fixed factors were estimated using type II Wald tests and random effects were esti- mated using likelihood-ratio test with one degree of freedom. Effects significant at P < 0.05 are in boldface type.

Article e01392; page 10 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

harder mericarps, and with longer or more numerous spines, often exhibited higher survival from finch preda- tion. The details of this finch-associated selection on defense traits varied over time in accordance with varia- tion in precipitation and changes in finch community

composition among islands, indicating that geographic variation in coevolutionary dynamics (sensu Thompson 2005) could be a source of phenotypic diversification in fruit morphology. Third, one of the traits examined, the presence of lower spines, exhibited divergence among

FIG. 6. Predicted seed survival probability for each mericarp trait estimated from logistic linear mixed-effects models in relation to (a) finch community composition and (b) year. The response variable used was binary, with 0 indicating mericarps with one or more seeds removed by finches, and 1 indicating complete mericarps with no seeds removed. Finch community composition was considered as a fixed binary factor, with 0 indicating the absence of the large-beaked finch species Geospiza magnirostris (only G. fortis present) and 1 indicating its presence. Shaded areas show 95% confidence intervals.

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 11

 

 

islands consistent with differences in finch community composition. Overall, our results are consistent with the interpretation that finches impose phenotypic selection on fruit morphological traits, and that these traits act as plant defenses in an ongoing coevolutionary arms race between Darwin’s finches and T. cistoides.

Patterns of temporal and spatial variation in seed predation by Darwin’s finches

We documented temporal and spatial variation in pre- dation on T. cistoides by finches, with predation rates being higher in 2015 and 2017 than in 2016. Temporal variation in seed predation is common in plants (e.g. Hulme 1994, Kolb et al. 2007), typically being attributed to temporal variation in biotic and abiotic factors (Hulme and Benkman 2002). On the Gal�apagos Islands, temporal variation is strongly influenced by cycles in precipitation, especially those attributable to the El Ni~no Southern Oscillation cycle. This variation in precipitation drives plant productivity in the arid zone (Porter 1979) where T. cistoides occurs. The abundance of preferred foods of Darwin’s finches (seeds, fruits, and insects) increases with higher precipitation (Grant and Boag 1980, Boag and Grant 1984, Price 1985, Gibbs and Grant 1987), which influences predation patterns of less-preferred seeds (Grant 1986, De Le�on et al. 2014, Grant and Grant 2014). Indeed, it has been shown that finches generally avoid T. cistoides in wet seasons and in particularly wet years (Boag and Grant 1981, Grant 1981). In accordance with these previous studies, our results suggest seed preda- tion of T. cistoides is mediated by variation in precipita- tion. We found that the lowest predation rate on T. cistoides occurred in 2016, which followed a year with high precipitation associated with an El Ni~no (wet) event;

whereas the highest predation rate occurred in 2017, fol- lowing a year with low precipitation associated with a La Ni~na (dry) event. However, we caution against over- interpretation of this finding because our observations correspond to a period of only 3 yr. In addition, temporal variation in finch predation on T. cistoides was not uni- form across islands, suggesting that features particular to each island might also shape the intensity of seed preda- tion; however, variation in precipitation within and among islands could not be included in our analysis, given that direct measurements of precipitation were only available from one population on Santa Cruz island. One intriguing possibility is that higher survival of T. cistoides seeds asso- ciated with years of high precipitation could be reinforced by a masting breeding strategy of T. cistoides. Although masting is a well-known mechanism in many tree species to increase survival of seeds by satiating predators (Janzen 1971, Silvertown 1980), this strategy has not been evalu- ated in T. cistoides. The observed spatial variation in seed predation is

likely also driven by a combination of biotic and abiotic factors. For example, we expected the highest rates of T. cistoides seed predation on islands with the large-beaked finch species G. magnirostris and G. conirostris. Our results were partially consistent with this expectation. In 2016, when predation rates on T. cis- toides were typically low, islands with large-beaked finch species indeed showed higher predation, but no effect of community composition was evident in other years. The smallest finch species that feeds on T. cistoides is G. for- tis (Grant 1981), but this finch prefers other food sources that are available following El Ni~no years. By contrast, large finches have less difficulty feeding on T. cistoides and they continue to feed on mericarps even following El Ni~no events. Thus, variation in seed predation can only be understood by looking at the

FIG. 7. Relationships between mericarp morphology and hardness. (a) Relationship between the global hardness estimate (PC1Global hardness) and a multivariate measure of mericarp size (PC1Size). Relationship between an estimate of hardness based on the three hardest locations on the mericarp (PC1Local hardness) and (b) mericarp length and (c) mericarp width. Regression lines are based on intercepts and slopes estimated from linear mixed models including island and population nested within island as random effects (see Statistical analyses).

Article e01392; page 12 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

interaction between finch community composition and temporal variation in climate.

Selection by Darwin’s finches on fruit traits of T. cistoides

Darwin’s finches were found to impose phenotypic selection on T. cistoides fruit defense traits. Mericarps sampled from natural populations that had lower spines, longer upper spines, and that were smaller, were more likely to survive predation. Finches might prefer larger mericarps because larger mericarps have

more seeds and thus represent a greater reward. Inter- estingly, we also found that mericarp size was inver- sely associated with mericarp hardness, which contributes to defense against ground finches (Boag and Grant 1981, Price et al. 1984). The ability of seeds or fruits to escape predation is generally thought to be greater for larger seeds (or fruits), for which leverage becomes more difficult, and harder for seeds (or fruits), which require more bite force to crack open (Abbott et al. 1977). However, we showed that smaller mericarps were harder than larger meri- carps, which suggests that small mericarps could be as

FIG. 8. Variation in Tribulus cistoides mericarp morphology. Means (circle) and standard error (bars) of each mericarp trait for the four islands that were sampled from 2015 to 2017: Floreana (Flo), San Crist�obal (S.Cri), Isabela (Isa), and Santa Cruz (S.Cru). Islands where large-beaked finch species are absent (only G. fortis present) are indicated in orange and islands where this species (i.e., Geospiza magnirostris) is present are indicated in black.

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 13

 

 

(or perhaps more) difficult to open than large meri- carps. Since finches commonly use specialized twisting motions to open mericarps (Grant 1981; Video S1), instead of just a direct biting effort, smaller mericarps also could require more precision and handling ability. The strength of selection varied over time and space,

as has been seen in other systems (Thompson 2005, Siepielski et al. 2009, 2013, Bell 2010). As with the observed temporal variation in seed predation, variation in selection on T. cistoides appeared to follow climatic cycles, although we do not yet know the causal links between precipitation and specific forms of selection. Furthermore, selection for longer upper spines and the presence of lower spines was stronger on islands where the large-beaked finch species were absent, perhaps because the largest beaked finch species (i.e., G. conirostris and G. magnirostris) are less deterred by T. cistoides defense traits. Stated in another way, the lar- gest species might have little difficulty opening even the most strongly defended T. cistoides mericarps. Once again, it is the interaction between finch community com- position and climate that appears to determine spatial and temporal variation in finch–T. cistoides inter- actions. Results from the short-term seed predation experi-

ment did not match our observations from natural pop- ulations. In the experiment, smaller mericarps were more likely to be preyed on and no association was evident between the presence of spines and mericarp predation.

These divergent results are perhaps not surprising since the experiment was conducted in only a single location and over a relatively short period of time (30 d), whereas the observational data capture data from many popula- tions over multiple years. Our experimental results, therefore, further emphasize the conditional nature of finch seed predation, and how selection varies through time. Evidence for phenotypic selection by Darwin’s finches

on T. cistoides fruits suggests a potential ongoing coevo- lutionary arms race between Darwin’s finches and T. cistoides. Our results thus add to previous studies in other systems showing that seed predators impose selec- tion on fruit morphology (e.g., Coffey et al. 1999, G�omez 2004); however, selection on T. cistoides fruit morphology has cascading implications in the Gal�apagos Islands (Fig. 9). Tribulus cistoides mericarps impose selection on the size and shape of the beak of G. fortis (Boag and Grant 1981, Boag and Grant 1984, Grant and Grant 1999), which drives episodic bouts of evolutionary change (Grant and Grant 2002, 2006). During dry periods, when small and soft seeds are scarce, larger beaked birds of G. fortis that are able to crack T. cistoides mericarps are favored when G. mag- nirostris are absent. However, when G. magnirostris are present, they compete with G. fortis for T. cistoides fruits, and cause an adaptive shift in G. fortis toward smaller beaks (Grant and Grant 2006). Therefore, the interaction between G. fortis and T. cistoides seems to be

FIG. 9. Ecological and evolutionary processes influencing interactions between Tribulus cistoides and Darwin’s finches. (1) Dry periods reduce seed diversity and abundance; (2) predation increases the year following La Ni~na years (low precipitation); (3) pres- ence of large-beaked finches increases seed predation the year following El Ni~no years (high precipitation); (4) large-beaked finches compete with Geospiza fortis; (5) decreased seed diversity/abundance leads to greater predation on T. cistoides; (6) decreased seed diversity/abundance reduces G. fortis population size; (7) decreased seed diversity/abundance selects for larger beaks of G. fortis when large-beaked bird species are absent, and smaller beaks when they are present; (8) selection for longer upper spines increases following El Ni~no years, whereas selection for the presence of lower spines and decreased size increase following La Ni~na years; (9) absence of large-beaked finch species leads to stronger selection for longer upper spines and for the presence of lower spines; (10) seed predation selects for longer upper spines and smaller mericarps (11); hypothesized coevolutionary arms race between T. cistoides and G. fortis. Interactions might also operate between the evolutionary processes and population dynamics within spe- cies (arrows not shown).

Article e01392; page 14 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

driven by reciprocal evolutionary changes that are medi- ated by temporal variation in La Ni~na/El Ni~no precipi- tation cycles and spatial (or temporal) variation in finch community composition. To further test this hypothesis, future research should focus on testing whether an adap- tive evolutionary response of T. cistoides fruits to finch predation modifies selection patterns imposed on finches’ beaks and affects their evolutionary trajectory.

Relationship between finch community and T. cistoides fruit morphology

Spatial variation in natural selection imposed by Dar- win’s finches has likely already caused adaptive diver- gence among island populations of T. cistoides. For example, the absence of lower spines in mericarps was associated with islands where the large-beaked finch spe- cies were absent. However, other traits examined (meri- carp length, width, and upper spine size) were not consistently associated with finch community composi- tion. The mismatch between selection pressure and pat- terns of variation of defense traits might have several causes. For instance, some defense traits might have low heritability, or opposing selective pressures, such as from dispersal and germination, which could mask the effects of seed predation on evolution (Primack 1987, Alc�an- tara and Rey 2003, Agrawal et al. 2013). In addition, fluctuating selection in space and time, as in the case of mericarp defense traits, coupled with gene flow, popula- tion bottlenecks, and founder events could constrain the translation of selection effect into morphological change, as predicted by the geographic mosaic of coevo- lution (Thompson 2005). Finally, it has been suggested that T. cistoides was introduced into the archipelago by humans (Porter 1967, Grant 1981), sometime after 1535, when the islands were discovered by Spanish explorers (Grant and Grant 2014). If true, it is possible that T. cis- toides has not yet had sufficient time, in combination with the above factors (e.g., founder effects, gene flow, opposing selection forces), to locally adapt to finch com- munity composition. However, the history of T. cistoides on the archipelago remains unresolved. The evolutionary response of fruit morphology in

T. cistoides to selection imposed by ground finches depends on several factors for which we still lack detailed information, such as heritability of fruit traits. Gal�apagos National Park restrictions prevented us from conducting common garden quantitative genetics experi- ments on T. cistoides; nonetheless, we detected variation among individual plants for almost all measured meri- carp traits. These results are consistent with the expecta- tion that variation in these traits is at least partially controlled by genetic variation. Future common garden experiments and genomic analyses would add to our understanding of the evolution of morphological defenses in T. cistoides. Key questions that could be addressed in future work include: What is the genetic structure and demographic history of T. cistoides

populations across the archipelago? Do trade-offs exist between natural selection imposed by finches and other potential drivers of selection on T. cistoides fruit mor- phology, such as dispersal, germination, and establish- ment? And, finally, is T. cistoides native to the islands or was this plant species introduced recently to the islands, possibly by humans?

CONCLUDING REMARKS

We report evidence that Darwin’s finches select T. cis- toides fruits based on defense traits, and that the varia- tion in selection patterns can be explained, in part, by finch community structure and variation in climate. Pre- vious work has suggested that predation on T. cistoides mericarps is an important agent of natural selection on finch beaks (Boag and Grant 1981, 1984, Grant and Grant 2006). We here suggest that a reciprocal process of natural selection by finches on mericarp morphology is also likely and, hence, that finches and T. cistoides are coevolving in an arms race. To inhibit finch predation, T. cistoides invests in physical defense structures, such as spines and mericarp hardness. In turn, the higher levels of defense in mericarps select for finches that are able to remove the seeds more efficiently. The specific process of reciprocal natural selection that leads to reciprocal adap- tation has yet to be directly documented, but the individ- ual component interactions make this scenario highly likely. In addition, considerable temporal variation in selection on mericarp defenses as well as finch beak mor- phology (Grant and Grant 2002), indicates that climatic conditions and spatial variation in finch communities mediate the ecological strength and evolutionary out- comes of this finch–plant interaction. Our work expands the understanding of ecological and

evolutionary interactions between Darwin’s finches and the plants whose seeds they eat. A long history of research, which includes Charles Darwin (1859), David Lack (1947), Grant and Grant (2014), and many other past and present researchers, has built a foundation for understand- ing the interplay between ecology and evolution from studying Darwin’s finches. We hope that our study sup- ports and inspires new avenues of research into these inter- actions.

ACKNOWLEDGMENTS

The study was performed with the logistical support of the Gal�apagos National Park (GNP) and Charles Darwin Research Station. The research permits to conduct the study were pro- vided by PNG (PC-29-14, PC-29-15, PC-42-16). Research fund- ing was kindly provided by SENESCYT-Ecuador, NEO program McGill-STRI, Department of Biology McGill, and Delise Alison Award from Redpath Museum to S. Carvajal- Endara; Natural Sciences and Engineering Research Council of Canada (NSERC) grants to A. P. Hendry and M. T. J. Johnson; NSF DEB-1553053 to N. C. Emery; CONACyT to D. Car- mona; NSERC Banting Postdoctoral Fellowship, Le Fonds Qu�eb�ecois de la Recherche sur la Nature et les Technologies postdoctoral research fellowship, Vineberg Fellowship McGill

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 15

 

 

University, Clare Hall Whitehead Fund, Christ’s College Gal�apagos Islands Visiting Scholarship Scheme, Phyllis and Eileen Gibbs Travelling Research Fellowship from Newnham College, and a British Ornithologists’ Union Research Grant to K. M. Gotanda; GAIAS-USFQ Grant to J. A. Chaves. Also, we thank Dieta Hanson for her assistance while performing a pilot seed predation experiments in 2014, and to Peter and Rosemary Grant for inspiring this work and patiently answering our many questions.

LITERATURE CITED

Abbott, I., L. K. Abbott, and P. R. Grant. 1977. Comparative ecology of Gal�apagos ground finches (Geospiza Gould): eval- uation of the importance of floristic diversity and interspeci- fic competition. Ecological Monographs 47:151–184.

Agrawal, A. A. 2011. Current trends in the evolutionary ecol- ogy of plant defence. Functional Ecology 25:420–432.

Agrawal, A. A., A. P. Hastings, M. T. J. Johnson, J. L. Maron, and J.-P. Salminen. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116.

Agrawal, A. A., M. T. J. Johnson, A. P. Hastings, and J. L. Maron. 2013. A field experiment demonstrating plant life-his- tory evolution and its eco-evolutionary feedback to seed predator populations. American Naturalist 181:S35–S45.

Alc�antara, J. M., and P. J. Rey. 2003. Conflicting selection pressures on seed size: evolutionary ecology of fruit size in a bird-dispersed tree, Olea europaea. Journal of Evolutionary Biology 16:1168–1176.

Barton, K. 2016. MuMIn: Multi-model inference, R package ver- sion 1.15. 6. https://CRAN.R-project.org/package=MuMIn

Bates, D., M. Maechler, B. Bolker, and S. C. Walker. 2015. Fit- ting linear mixed-effects models using lme4. Journal of Statis- tical Software 67:1–48.

Bell, G. 2010. Fluctuating selection: the perpetual renewal of adaptation in variable environments. Philosophical Transac- tions of the Royal Society B 365:87–97.

Boag, P. T., and P. R. Grant. 1981. Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Gal�apagos. Science 214:82–85.

Boag, P. T., and P. R. Grant. 1984. Darwin’s finches (Geospiza) on Isla Daphne Major, Gal�apagos: breeding and feeding ecol- ogy in a climatically variable environment. Ecological Mono- graphs 54:463–489.

Buddenhagen, C., and K. J. Jewell. 2006. Invasive plant seed viability after processing by some endemic Gal�apagos birds. Ornitolog�ıa Neotropical 17:73–80.

Carmona, D., M. J. Lajeunesse, and M. T. J. Johnson. 2011. Plant traits that predict resistance to herbivores. Functional Ecology 25:358–367.

Coffey, K., C. W. Benkman, and B. G. Milligan. 1999. The adaptive significance of spines on pine cones. Ecology 80:1221–1229.

Crawley, M. J. 1983. Herbivory: the dynamics of animal-plant interactions. University of California Press, Berkeley, Califor- nia, USA.

Darwin, C. R. 1859. On the origin of species by means of natu- ral selection, or the preservation of favoured races in the struggle for life. John Murray, London, UK.

De Le�on, L. F., J. Raeymaekers, E. Bermingham, J. Podos, A. Herrel, and A. P. Hendry. 2011. Exploring possible human influences on the evolution of Darwin’s finches. Evolution 65:2258–2272.

De Le�on, L. F., J. Podos, T. Gardezi, A. Herrel, and A. P. Hen- dry. 2014. Darwin’s finches and their diet niches: the

sympatric coexistence of imperfect generalists. Journal of Evolutionary Biology 27:1093–1104.

Didiano, T. J., N. E. Turley, G. Everwand, H. Schaefer, M. J. Crawley, and M. T. J. Johnson. 2014. Experimental test of plant defence evolution in four species using long-term rabbit exclosures. Journal of Ecology 102:584–594.

Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586–608.

Fritz, R. S., and E. L. Simms. 1992. Plant resistance to herbi- vores and pathogens: ecology, evolution and genetics. Univer- sity of Chicago Press, Chicago, Illinois, USA.

Geist, D. 1996. On the emergence and submergence of the Gal�apagos Islands, Ecuador. Noticias de Gal�apagos 56:5.

Gibbs, H. L., and P. R. Grant. 1987. Ecological consequences of an exceptionally strong El Ni~no event on Darwin’s finches. Ecology 68:1735–1746.

G�omez, J. M. 2004. Bigger is not always better: conflicting selec- tive pressures on seed size in Quercus ilex. Evolution 58:71–80.

Grant, P. R. 1981. The feeding of Darwin’s finches on Tribulus cistoides (L.) seeds. Animal Behaviour 29:785–793.

Grant, P. R. 1986. Ecology and evolution of Darwin’s finches. Princeton University Press, Princeton, New Jersey, USA.

Grant, P. R. 1999. Ecology and evolution of Darwin’s finches. Second edition. Princeton University Press, Princeton, New Jersey, USA.

Grant, P. R., and P. T. Boag. 1980. Rainfall on the Galapagos and the demography of Darwin’s finches. Auk 97:227–244.

Grant, P. R., and K. T. Grant. 1979. The breeding and feeding of the Gal�apagos dove, Zenaida galapagoensis. Condor 81:397–403.

Grant, B. R., and P. R. Grant. 1982. Niche shifts and competi- tion in Darwin’s finches: Geospiza conirostris and congeners. Evolution 36:637–657.

Grant, P. R., and B. R. Grant. 1995. Predicting microevolution- ary responses to directional selection on heritable variation. Evolution 49:241–251.

Grant, P. R., and B. R. Grant. 2002. Unpredictable evolu- tion in a 30-year study of Darwin’s finches. Science 296:707–711.

Grant, P. R., and B. R. Grant. 2006. Evolution of character dis- placement in Darwin’s finches. Science 313:224–226.

Grant, P. R., and B. R. Grant. 2014. 40 Years of evolution: Dar- win’s finches on Daphne major island. Princeton University Press, Princeton, New Jersey, USA.

Guerrero, A. M., and A. Tye. 2009. Darwin’s finches as seed predators and dispersers. Wilson Journal of Ornithology 121:752–764.

Holm, L. G., D. L. Plucknett, J. V. Pancho, and J. P. Herberger. 1977. The World’s Worst Weeds. Distribution and Biology. University Press of Hawaii, Honolulu, Hawaii, USA.

Hulme, P. E. 1994. Post-dispersal seed predation in grassland: its magnitude and sources of variation. Journal of Ecology 82:645–652.

Hulme, P. E., and C. W. Benkman. 2002. Granivory. Pages 132–154 in C. Herrera and O. Pellmyr, editors. Plant-animal interactions: an evolutionary approach. Blackwell Scientific Publications, New York, New York, USA.

Janzen, D. H. 1971. Seed predation by animals. Annual Review of Ecology and Systematics 2:465–492.

Janzen, F. J., and H. S. Stern. 1998. Logistic regression for empiri- cal studies of multivariate selection. Evolution 52:1564–1571.

Karban, R., and A. A. Agrawal. 2002. Herbivore offense. Annual Review of Ecology and Systematics 33:641–664.

Kolb, A., J. Ehrl�en, and O. Eriksson. 2007. Ecological and evo- lutionary consequences of spatial and temporal variation in pre-dispersal seed predation. Perspectives in Plant Ecology, Evolution and Systematics 9:79–100.

Article e01392; page 16 SOF�IA CARVAJAL-ENDARA ET AL. Ecological Monographs Vol. 90, No. 1

 

 

Lack, D. 1947. Darwin’s finches. Cambridge University Press, Cambridge, UK.

Lande, R., and S. J. Arnold. 1983. The measurement of selec- tion on correlated characters. Evolution 37:1210–1226.

Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfin- ger. 1996. SAS system for mixed models. SAS Institute, Cary, North Carolina, USA.

Pampush, J. D., D. J. Daegling, A. E. Vick, W. S. McGraw, R. M. Covey, and A. J. Rapoff. 2011. Converting durometer data into elastic modulus in biological materials. American Jour- nal of Physical Anthropology 146:650–653.

Paterson, S., et al. 2010. Antagonistic coevolution accelerates molecular evolution. Nature 464:275.

Porter, D. M. 1967. Another Tribulus adventive in the New World. Rhodora 69:455–456.

Porter, D. M. 1971. Notes on the floral glands in Tribulus (Zygo- phyllaceae). Annals of the Missouri Botanical Garden 58:1–5.

Porter, D. M. 1972. The genera of Zygophyllaceae in the south- eastern United States. Journal of the Arnold Arboretum 53:531–552.

Porter, D. M. 1979. Endemism and evolution in Galapagos Islands vascular plants. Pages 225–256 in D. Bramwell, editor. Plants and Islands. Academic Press, London, UK.

Price, T. 1985. Reproductive responses to varying food supply in a population of Darwin’s finches: clutch size, growth rates and hatching synchrony. Oecologia 66:411–416.

Price, T. 1987. Diet variation in a population of Darwin’s finches. Ecology 68:1015–1028.

Price, T. D., P. R. Grant, H. L. Gibbs, and P. T. Boag. 1984. Recurrent patterns of natural selection in a population of Darwin’s finches. Nature 309:787–789.

Primack, R. B. 1987. Relationships among flowers, fruits, and seeds. Annual Review of Ecology and Systematics 18:409–430.

R Core Team. 2017. R: A language and environment for statisti- cal computing. R Foundation for Statistical Computing, Vienna, Austria.

Schluter, D., and P. R. Grant. 1984. Determinants of morpho- logical patterns in communities of Darwin’s finches. Ameri- can Naturalist 123:175–196.

Siepielski, A. M., J. D. DiBattista, and S. M. Carlson. 2009. It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecology Letters 12:1261–1276.

Siepielski, A. M., K. M. Gotanda, M. B. Morrissey, S. E. Dia- mond, J. D. DiBattista, and S. M. Carlson. 2013. The spatial patterns of directional phenotypic selection. Ecology Letters 16:1382–1392.

Silvertown, J. W. 1980. The evolutionary ecology of mast seeding in trees. Biological Journal of the Linnean Society 14: 235–250.

Stramma, L., T. Fischer, D. S. Grundle, G. Krahmann, H. W. Bange, and C. A. Marandino. 2016. Observed El Ni~no condi- tions in the eastern tropical Pacific in October 2015. Ocean Science 12:861–873.

Thompson, J. N. 1999. The evolution of species interactions. Science 284:2116–2118.

Thompson, J. N. 2005. The geographic mosaic of coevolution. University of Chicago Press, Chicago, Illinois, USA.

Vamosi, S. M. 2005. On the role of enemies in divergence and diversification of prey: a review and synthesis. Canadian Journal of Zoology 83:894–910.

Wiggins, I. L., and D. M. Porter. 1971. Flora of the Gal�apagos Islands. Stanford University Press, Stanford, California, USA.

Z€ust, T., C. Heichinger, U. Grossniklaus, R. Harrington, D. J. Kliebenstein, and L. A. Turnbull. 2012. Natural enemies drive geographic variation in plant defenses. Science 338: 116–119.

SUPPORTING INFORMATION

Additional supporting information may be found online at: http://onlinelibrary.wiley.com/doi/10.1002/ecm.1392/full

DATA AVAILABILITY

Data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.qq4715f

February 2020 DARWIN’S FINCHES AS AGENTS OF SELECTION Article e01392; page 17

 

 

Copyright of Ecological Monographs is the property of John Wiley & Sons, Inc. and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder’s express written permission. However, users may print, download, or email articles for individual use.