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Rolshausen, Gregor; Phillip, Dawn A. T.; Beckles, Denise M.; Akbari, Ali; Ghoshal, Subhasis; Hamilton, Patrick B.; Tyler, Charles R.; Scarlett, Alan G.; Ramnarine, Indar; Bentzen, Paul; Hendry, Andrew P. 2015-06-16 The ability of populations to rapidly adapt to new environments will determine their future in an increasingly human-modified world. Although meta-analyses do frequently uncover signatures of local adaptation, they also reveal many exceptions. We suggest that particular constraints on local adaptation might arise when organisms are exposed to novel stressors, such as anthropogenic pollution. To inform this possibility, we studied the extent to which guppies (Poecilia reticulata) show local adaptation to oil pollution in southern Trinidad. Neutral genetic markers revealed that paired populations in oil-polluted versus not-polluted habitats diverged independently in two different watersheds. Morphometrics revealed some divergence (particularly in head shape) between these environments, some of which was parallel between rivers. Reciprocal transplant experiments in nature, however, found little evidence of local adaptation based on survival and growth. Moreover, subsequent laboratory experiments showed that the two populations from oil-polluted sites showed only weak local adaptation even when compared to guppies from oil-free northern Trinidad. We conclude that guppies show little local adaptation to oil pollution, which might result from the challenges associated with adaptation to particularly stressful environments. It might also reflect genetic drift owing to small population sizes and/or high gene flow between environments.
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De León, Luis F.; Podos, Jeffrey; Gardezi, Tariq; Herrel, Anthony; Hendry, Andrew P. 2014-07-21 Adaptive radiation can be strongly influenced by interspecific competition for resources, which can lead to diverse outcomes ranging from competitive exclusion to character displacement. In each case, sympatric species are expected to evolve into distinct ecological niches, such as different food types, yet this expectation is not always met when such species are examined in nature. The most common hypotheses to account for the coexistence of species with substantial diet overlap rest on temporal variation in niches (often diets). Yet spatial variation in niche overlap might also be important, pointing to the need for spatiotemporal analyses of diet and diet overlap between closely related species persisting in sympatry. We here perform such an analysis by characterizing the diets of, and diet overlap among, four sympatric Darwin's ground finch species at three sites and over 5 years on a single Galápagos island (Santa Cruz). We find that the different species have broadly similar and overlapping diets – they are to some extent generalists and opportunists – yet we also find that each species retains some ‘private’ resources for which their morphologies are best suited. Importantly, use of these private resources increased considerably, and diet overlap decreased accordingly, when the availability of preferred shared foods, such as arthropods, was reduced during drought conditions. Spatial variation in food resources was also important. These results together suggest that the ground finches are ‘imperfect generalists’ that use overlapping resources under benign conditions (in space or time), but then retreat to resources for which they are best adapted during periods of food limitation. These conditions likely promote local and regional coexistence.
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Gotanda, Kiyoko M.; Correa, Cristián; Turcotte, Martin M.; Rolshausen, Gregor; Hendry, Andrew P. 2015-03-19 Cope's rule, wherein a lineage increases in body size through time, was originally motivated by macro-evolutionary patterns observed in the fossil record. More recently, some authors have argued that evidence exists for generally positive selection on individual body size in contemporary populations, providing a micro-evolutionary mechanism for Cope's rule. If larger body size confers individual fitness advantages as the selection estimates suggest, thereby explaining Cope's rule, then body size should increase over micro-evolutionary time scales. We test this corollary by assembling a large database of studies reporting changes in phenotypic body size through time in contemporary populations, as well as studies reporting average breeding values for body size through time. Trends in body size were quite variable with an absence of any general trend, and many populations trended toward smaller body sizes. Although selection estimates appear to support Cope's rule, our results suggest that actual rates of phenotypic change for body size do not. We discuss potential reasons for this discrepancy and its implications for the understanding of Cope's rule.
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Haller, Benjamin C.; de Vos, Jurriaan M.; Keller, Barbara; Hendry, Andrew P.; Conti, Elena 2015-07-16 The evolution of the flower is commonly thought to have spurred angiosperm diversification. Similarly, particular floral traits might have promoted diversification within specific angiosperm clades. We hypothesize that traits promoting the precise positional transfer of pollen between flowers might promote diversification. In particular, precise pollen transfer might produce partial reproductive isolation that facilitates adaptive divergence between parapatric populations differing in their reproductive-organ positions. We investigate this hypothesis with an individual-based model of pollen transfer dynamics associated with heterostyly, a floral syndrome that depends on precise pollen transfer. Our model shows that precise pollen transfer can cause sexual selection leading to divergence in reproductive-organ positions between populations served by different pollinators, pleiotropically causing an increase in reproductive isolation through a “magic trait” mechanism. Furthermore, this increased reproductive isolation facilitates adaptive divergence between the populations in an unlinked, ecologically selected trait. In a different pollination scenario, however, precise pollen transfer causes a decrease in adaptive divergence by promoting asymmetric gene flow. Our results highlight the idea that magic traits are not “magic” in isolation; in particular, the effect size of magic traits in speciation depends on the external environment, and also on other traits that modify the strength of the magic trait's influence on non-random mating. Overall, we show that the evolutionary consequences of pollen transfer dynamics can depend strongly on the available pollinator fauna and on the morphological fit between flowers and pollinators. Furthermore, our results illustrate the potential importance of even weak reproductive isolating barriers in facilitating adaptive divergence. https://creativecommons.org/publicdomain/zero/1.0/
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Kaeuffer, Renaud; Peichel, Catherine Lynn; Bolnick, Daniel I.; Hendry, Andrew P. 2011-08-04 Convergent (or parallel) evolution provides strong evidence for a deterministic role of natural selection: similar phenotypes evolve when independent populations colonize similar environments. In reality, however, independent populations in similar environments always show some differences: some non-convergent evolution is present. It is therefore important to explicitly quantify the convergent and non-convergent aspects of trait variation, and to investigate the ecological and genetic explanations for each. We performed such an analysis for threespine stickleback (Gasterosteus aculeatus) populations inhabiting lake and stream habitats in independent watersheds. Morphological traits differed in the degree to which lake-stream divergence was convergent across watersheds. Some aspects of this variation were correlated with ecological variables related to diet, presumably reflecting the strength and specifics of divergent selection. Furthermore, a genetic scan revealed some markers that diverged between lakes and streams in many of the watersheds and some that diverged in only a few watersheds. Moreover, some of the lake-stream divergence in genetic markers was associated within some of the lake-stream divergence in morphological traits. Our results suggest that convergent evolution, and deviations from it, are primarily the result of natural selection, which corresponds in only some respect to the dichotomous habitat classifications frequently used in such studies.
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Gotanda, Kiyoko M.; Pack, Amy; Leblond, Caroline; Hendry, Andrew P. 2019-09-11 The Trinidadian guppy is emblematic of parallel and convergent evolution, with repeated demonstrations that predation regime is a driver of adaptive trait evolution. A classic and foundational experiment in this system was conducted by John Endler 40 years ago, where male guppies placed into low-predation environments in the laboratory evolved increased color in a few generations. However, Endler’s experiment did not employ the now typical design for a parallel/convergent evolution study, which would employ replicates of different ancestral lineages. We therefore implemented an experiment that seeded replicate mesocosms with small founding populations of guppies originating from high-predation populations of two very different lineages. The different mesocosms were maintained identically, and male guppy color was quantified every four months. After one year, we tested whether male colour had increased, whether replicates within a lineage had parallel phenotypic trajectories, and whether the different lineages converged on a common phenotype. Results showed that male guppy color generally increased through time, primarily due to changes in melanic color; whereas the other colors showed inconsistent and highly variable trajectories. Most of the non-parallelism in phenotypic trajectories was among mesocosms containing different lineages. In addition to this mixture of parallelism and non-parallelism, convergence was not evident in that the variance in colour among the mesocosms actually increased through time. We suggest that our results reflect the importance of high variation in female preference and founder effects, both of which could be important in nature.
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Hanson, Dieta; Moore, Jean-Sébastien; Taylor, Eric B.; Barrett, Rowan D.H.; Hendry, Andrew P.; Moore, J.-S.; Barrett, R. D. H. 2016-09-08 Ecological speciation occurs when populations evolve reproductive isolation as a result of divergent natural selection. This isolation can be influenced by many potential reproductive barriers, including selection against hybrids, selection against migrants, and assortative mating. How and when these barriers act and interact in nature is understood for relatively few empirical systems. We used a mark-recapture experiment in a contact zone between lake and stream three-spined sticklebacks (Gasterosteus aculeatus, Linnaeus) to evaluate the occurrence of hybrids (allowing inferences about reproductive isolation), the inter-annual survival of hybrids (allowing inferences about selection against hybrids), and the shift in lake-like versus stream-like characteristics (allowing inferences about selection against migrants). Genetic and morphological data suggest the occurrence of hybrids and no selection against hybrids in general, a result contradictory to a number of other studies of sticklebacks. However, we did find selection against more lake-like individuals, suggesting a barrier to gene flow from the lake into the stream. Combined with previous work on this system, our results suggest that multiple (most weakly and often asymmetric) barriers must be combining to yield substantial restrictions on gene flow. This work provides evidence of a reproductive barrier in lake-stream sticklebacks and highlights the value of assessing multiple reproductive barriers in natural contexts. https://creativecommons.org/publicdomain/zero/1.0/
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Blondel, Léa; Baillie, Lyndsey; Quinton, Jessica; Alemu, Jahson B.; Paterson, Ian; Hendry, Andrew P.; Bentzen, Paul 2019-04-01 In dendritic river systems, gene flow is expected to occur primarily within watersheds. Yet, rare cross‐watershed transfers can also occur, whether mediated by (often historical) geological events or (often contemporary) human activities. We explored these events and their potential evolutionary consequences by analyzing patterns of neutral genetic variation (microsatellites) and adaptive phenotypic variation (male color) in wild guppies (Poecilia reticulata) distributed across two watersheds in northern Trinidad. We found the expected signatures of within‐watershed gene flow; yet we also inferred at least two instances of cross‐watershed gene flow—one in the upstream reaches and one further downstream. The upstream cross‐watershed event appears to be very recent (41 ± 13 years), suggesting dispersal via recent flooding or undocumented human‐mediated transport. The downstream cross‐watershed event appears to be considerably older (577 ± 265 years), suggesting a role for rare geological or climatological events. Alongside these strong signatures of both contemporary and historical gene flow, we found little evidence of impacts on presumably adaptive phenotypic differentiation, except perhaps in the one instance of very recent cross‐watershed gene flow. Selection in this system seems to overpower gene flow—at least on the spatiotemporal scales investigated here.
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Dargent, Felipe; Chen, Lisa; Fussmann, Gregor F.; Ghalambor, Cameron K.; Hendry, Andrew P. 2018-12-19 Progress toward local adaptation is expected to be enhanced when divergent selection is multi-dimensional, because many simultaneous sources of selection can increase the total strength of selection and enhance the number of independent traits under selection. Yet, whether local adaptation ensues from multi-dimensional selection also depends on its potential to cause the build-up of reproductive barriers such as sexual signals and preference for these signals. We used replicate experimental introductions of guppies (Poecilia reticulata) in nature to test whether an abrupt and dramatic shift in multiple important ecological dimensions (at a minimum: parasitism, predation, and diet/resources) promoted the contemporary evolution of assortative mating. After 8-12 post-introduction guppy generations in the wild, we bred descendants of each population in a common-garden laboratory environment for two generations, after which we recorded the preferences of females from each population for males from each population. We found contemporary evolution of male traits (size, body condition, colour) that should influence mate choice, but no evidence for the occurrence of positive assortative preferences. That is, females in a given evolving population did not prefer males from that population over males from other populations. Instead, females tended to prefer novel males (i.e. disassortative mating), which likely acts as a mechanism preventing the evolution of reproductive isolation. Preferences for novelty may explain why many cases of local adaptation do not lead to the evolution of reproductive barriers and ecological speciation.
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Borealis
Beausoleil, Marc-Olivier; Carrión-Avilés, Paola; Podos, Jeffrey; Camacho, Carlos; Rabadán-González, Julio; Richard, Roxanne; Lalla, Kristen; Raeymaekers, Joost A. M.; Knutie, Sarah A.; De León, Luis F.; Chaves, Jaime A.; Clayton, Dale H.; Koop, Jennifer A. H.; Sharpe, Diana M. T.; Gotanda, Kiyoko M.; Huber, Sarah K.; Barrett, Rowan D. H.; Hendry, Andrew P. 2023-08-22 <h3>Purpose</h3> The dataset and script were developed to <ol> <li>estimate the fitness landscape for Darwin's ground finch species (<i>Geospiza</i> spp.) at El Garrapatero over 2003 to 2020, and </li> <li> use the fitness landscape to consider theoretical expectations and previous empirical assertions regarding the topology of fitness and adaptive landscapes. </li> </ol> <h3>Brief Methodology</h3> To fulfil these aims, we used the data from our long-term monitoring site El Garrapatero on Santa Cruz in the Galápagos, Ecuador. We calculated lifespan as a fitness proxi from our recapture data to construct a fitness and adaptive landscape using the beak length and depth. <h3>Data</h3> Please, download and consult the <i>README</i> text file which explains the contents of <i>adaptive.landscapes.finches.zip</i>. The <i>.zip</i> file preserves the folder structure needed to run the scripts. The main program needed for the analysis is <a href="https://cran.r-project.org">R (open-source)</a>, but to fully reproduce all the code, <a href="https://imagemagick.org/index.php">ImageMagick (open-source)</a> and <a href="https://ffmpeg.org">FFMPEG (open-source)</a> programs. <h3>References</h3> <ul> <li><a href="https://github.com/beausoleilmo/adaptive.landscapes.finches">GitHub repository of 'adaptive.landscapes.finches'</a> </li> <li>The scripts and data and for the R language (R Core Team 2023; R version, 4.2.1 (Funny-Looking Kid)). </li> </ul>
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Dryad
Paccard, Antoine; Wasserman, Ben A.; Hanson, Dieta; Astorg, Louis; Durston, Dan; Kurland, Sara; Apgar, Travis M.; El-Sabaawi, Rana W.; Palkovacs, Eric P.; Hendry, Andrew P.; Barrett, Rowan D.H.; Barrett, Rowan D. H. 2018-03-06 The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar-built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re-form within a few weeks or months, thereby re-isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within-population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure, and then analyzed how stickleback armor traits, the associated genes Eda and Pitx1, and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among-population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within-population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype, and the presence of predators; thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within-population variation while reducing, but not eliminating, among-population variation driven by spatial environmental variation.
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De León, Luis Fernando; Raeymaekers, Joost A.M.; Bermingham, Eldredge; Podos, Jeffrey; Herrel, Anthony; Hendry, Andrew P. 2011-11-08 Humans are an increasingly common influence on the evolution of natural populations. Potential arenas of influence include altered evolutionary trajectories within populations and modifications of the process of divergence among populations. We consider this second arena in the medium ground finch (Geospiza fortis) on Santa Cruz Island, Galápagos, Ecuador. Our study compared the G. fortis population at a relatively undisturbed site, El Garrapatero, to the population at a severely disturbed site, Academy Bay, which is immediately adjacent to the town of Puerto Ayora. The El Garrapatero population currently shows beak size bimodality that is tied to assortative mating and disruptive selection, whereas the Academy Bay population was historically bimodal but has lost this property in conjunction with a dramatic increase in local human population density. We here evaluate potential ecological-adaptive drivers of the differences in modality by quantifying relationships between morphology (beak and head dimensions), functional performance (bite force), and environmental characteristics (diet). Our main finding is that associations among these variables are generally weaker at Academy Bay than at El Garrapatero, possibly because novel foods are used at the former site irrespective of individual morphology and performance. These results are consistent with the hypothesis that the rugged adaptive landscapes promoting and maintaining diversification in nature can be smoothed by human activities, thus hindering ongoing adaptive radiation.
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Oke, Krista B.; Bukhari, Mehvish; Kaeuffer, Renaud; Rolshausen, Gregor; Räsänen, Katja; Bolnick, Daniel I.; Peichel, Catherine L.; Hendry, Andrew P. 2015-09-28 Parallel (and convergent) phenotypic variation is most often studied in the wild, where it is difficult to disentangle genetic versus environmentally-induced effects. As a result, the potential contributions of phenotypic plasticity to parallelism (and non-parallelism) are rarely evaluated in a formal sense. Phenotypic parallelism could be enhanced by plasticity that causes stronger parallelism across populations in the wild than would be expected from genetic differences alone. Phenotypic parallelism could be dampened if site-specific plasticity induced differences between otherwise genetically-parallel populations. We used a common-garden study of three independent lake-stream stickleback population pairs to evaluate the extent to which adaptive divergence has a genetic or plastic basis, and to investigate the enhancing versus dampening effects of plasticity on phenotypic parallelism. We found that lake-stream differences in most traits had a genetic basis, but that several traits also showed contributions from plasticity. Moreover, plasticity was much more prevalent in one watershed than in the other two. In most cases, plasticity enhanced phenotypic parallelism, whereas in a few cases plasticity had a dampening effect. Genetic and plastic contributions to divergence seem to play a complimentary, likely adaptive, role in phenotypic parallelism of lake-stream stickleback. These findings highlight the value of formally comparing wild-caught and lab-reared individuals in the study of phenotypic parallelism.
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Leigh, Deborah M.; Hendry, Andrew P.; Vázquez-Domínguez, Ella; Friesen, Vicki L. 2019-04-30 Genetic variation is fundamental to population fitness and adaptation to environmental change. Human activities are driving declines in many wild populations and could have similar effects on genetic variation. Despite the importance of estimating such declines, no global estimate of the magnitude of ongoing genetic variation loss has been conducted across species. By combining studies that quantified recent changes in genetic variation across a mean of 27 generations for 91 species, we conservatively estimate a 5.4-6.5% decline in within-population genetic diversity of wild organisms since the industrial revolution. This loss has been most severe for island species, which show a 30% average decline. We identified taxonomic and geographic gaps in temporal studies that must be urgently addressed. Our results are consistent with single time-point meta-analyses, which indicated that genetic variation is likely declining. However, our results represent the first confirmation of a global decline, and provide an estimate of the magnitude of the genetic variation lost from wild populations.
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Hendry, Andrew P.; Kaeuffer, Renaud; Crispo, Erika; Peichel, Catherine Lynn; Bolnick, Daniel I. 2013-06-05 Evolutionary inferences are usually based on statistical models that compare mean genotypes and phenotypes (or their frequencies) among populations. An alternative is to use the actual distribution of genotypes and phenotypes to infer the “exchangeability” of individuals among populations. We illustrate this approach by using discriminant functions on principal components to classify individuals among paired lake and stream populations of threespine stickleback in each of six independent watersheds. Classification based on neutral and non-neutral microsatellite markers was highest to the population of origin and next-highest to populations in the same watershed. These patterns are consistent with the influence of historical contingency (separate colonization of each watershed) and subsequent gene flow (within but not between watersheds). In comparison to this low genetic exchangeability, ecological (diet) and morphological (trophic and armor traits) exchangeability was relatively high – particularly among populations from similar habitats. These patterns reflect the role of natural selection in driving parallel changes adaptive changes when independent populations colonize similar habitats. Importantly, however, substantial non-parallelism was also evident. Our results show that analyses based on exchangeability can confirm inferences based on statistical analyses of means or frequencies, while also refining insights into the drivers of – and constraints on – evolutionary diversification.
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Carvajal-Endara, Sofía; Hendry, Andrew P.; Emery, Nancy C.; Davies, T. Jonathan 2018-01-31 Remote locations, such as oceanic islands, typically harbour relatively few species, some of which go on to generate endemic radiations. Species colonising these locations tend to be a non-random subset from source communities, which is thought to reflect dispersal limitation. However, non-random colonisation could also result from habitat filtering, whereby only a few continental species can become established. We evaluate the imprints of these processes on the Galápagos flora by analysing a comprehensive regional phylogeny for ~ 39 000 species alongside information on dispersal strategies and climatic suitability. We found that habitat filtering was more important than dispersal limitation in determining species composition. This finding may help explain why adaptive radiation is common on oceanic archipelagoes – because colonising species can be relatively poor dispersers with specific niche requirements. We suggest that the standard assumption that plant communities in remote locations are primarily shaped by dispersal limitation deserves reconsideration.
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Haller, Benjamin C.; Hendry, Andrew P. 2013-09-12 Despite the potential for rapid evolution, stasis is commonly observed over geological timescales – the so-called “paradox of stasis.” This paradox would be resolved if stabilizing selection were common, but stabilizing selection is infrequently detected in natural populations. We hypothesize a simple solution to this apparent disconnect: stabilizing selection is hard to detect empirically once populations have adapted to a fitness peak. To test this hypothesis, we developed an individual-based model of a population evolving under an invariant stabilizing fitness function. Stabilizing selection on the population was infrequently detected in an “empirical” sampling protocol, because (1) trait variation was low relative to the fitness peak breadth; (2) non-selective deaths masked selection; (3) populations wandered around the fitness peak; and (4) sample sizes were typically too small. Moreover, the addition of negative frequency-dependent selection further hindered detection by flattening or even dimpling the fitness peak, a phenomenon we term “squashed stabilizing selection”. Our model demonstrates that stabilizing selection provides a plausible resolution to the paradox of stasis despite its infrequent detection in nature. The key reason is that selection “erases its traces”: once populations have adapted to a fitness peak, they are no longer expected to exhibit detectable stabilizing selection.
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Carvajal-Endara, Sofía; Hendry, Andrew P.; Emery, Nancy C.; Neu, Corey P.; Carmona, Diego; Gotanda, Kiyoko M.; Davies, T. Jonathan; Chaves, Jaime A.; Johnson, Marc T. J 2020-01-13 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 are a potent agent of selection that drives contemporary evolutionary change in finch beak morphology. Although the effects of these interaction 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 varies 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 three years. 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 inter-annual 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.

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