The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine

The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary cold-spots).     

Interactions among moths, crossbills, squirrels, and lodgepole pine in a geographic selection mosaic

Repeated patterns among biological communities suggest similar evolutionary and ecological forces are acting on the communities. Conversely, the lack of such patterns suggests that similar forces are absent or additional ones are present. Coevolution between a seed predator, the red crossbill (Loxia curvirostra complex), and lodgepole pine (Pinus contorta var. latifolia) exemplifies the ecological and evolutionary predictions for coevolving systems. In the absence of another seed predator and preemptive competitor (pine squirrels Tamiasciurus hudsonicus), natural selection by crossbills results in the evolution of larger cones with thicker distal scales, while relaxation of selection by squirrels results in the evolution of cones with more seeds and a greater ratio of seed mass to cone mass. However, in one range, the Little Rocky Mountains, distal scale thickness has diverged as expected but cone size has not. In these mountains seed predation by lodgepole pine cone borer moths (Eucosma recissoriana) was about 10 times greater than in other ranges lacking squirrels. We quantified moth predation and cone traits and found that moths select for smaller cones with fewer seeds. Thus, selection by moths in the Little Rocky Mountains counters both selection by crossbills for large cone size and relaxation of selection by squirrels favoring more seeds per cone and accounts for the relatively small and few-seeded cones in these mountains. It is also apparent that selection by crossbills changes seed defenses in a manner that favors seed predation by moths, whereas selection by squirrels likely reduces such predation. These results demonstrate the importance of considering the evolutionary consequences of community context in locally evolved (coevolved) traits and interactions.     

Local co-adaptation leading to a geographical mosaic of coevolution in a social parasite system

The geographical mosaic theory of coevolution predicts differences in the advance or trajectory of the coevolutionary process between local communities due to their composition and the strength of ecological selection pressures through competition and resource availability. In this study, we investigate local co-adaptation in different populations of a social parasite. We conducted cross-fostering experiments to test for interpopulational differences in raiding efficiency between various populations of a slave-making ant and the defence abilities of local hosts. Here, we demonstrate that the success of raids strongly depends on the combination of populations of the parasite Harpagoxenus sublaevis and its host Leptothorax acervorum, indicating very localized coevolution. We found no absolute differences between slave-maker populations; the outcome of an encounter depended more on whether the two opponents occur in sympatry or allopatry. Furthermore, this study supports the results of our earlier work, that the unparasitized English L. acervorum population is most aggressive against the parasite.     

Geographic variation in the evolution and coevolution of a tritrophic interaction

The geographic mosaic theory of coevolution predicts that geographic variation in species interactions will lead to differing selective pressures on interacting species, producing geographic variation in the traits of interacting species (Thompson 2005). We supported this hypothesis in a study of the geographic variation in the interactions among Eurosta solidaginis and its natural enemies. Eurosta solidaginis is a fly (Diptera: Tephritidae) that induces galls on subspecies of tall goldenrod, Solidago altissima altissima and S. a. gilvocanescens. We measured selection on E. solidaginis gall size and shape in the prairie and forest biomes in Minnesota and North Dakota over an 11-year period. Galls were larger and more spherical in the prairie than in the forest. We supported the hypothesis that the divergence in gall morphology in the two biomes is due to different selection regimes exerted by natural enemies of E. solidaginis. Each natural enemy exerted similar selection on gall diameter in both biomes, but differences in the frequency of natural enemy attack created strong differences in overall selection between the prairie and forest. Bird predation increased with gall diameter, creating selection for smaller-diameter galls. A parasitic wasp, Eurytoma gigantea, and Mordellistena convicta, an inquiline beetle, both caused higher E. solidaginis mortality in smaller galls, exerting selection for increased gall diameter. In the forest there was stabilizing selection on gall diameter due to a combination of bird predation on larvae in large galls, and M. convicta- and E. gigantea-induced mortality on larvae in small galls. In the prairie there was directional selection for larger galls due to M. convicta and E. gigantea mortality on larvae in small galls. Mordellistena convicta-induced mortality was consistently higher in the prairie than in the forest, whereas there was no significant difference in E. gigantea-induced mortality between biomes. Bird predation was nonexistent in the prairie so the selection against large galls found in the forest was absent. We supported the hypothesis that natural enemies of E. solidaginis exerted selection for spherical galls in both biomes. In the prairie M. convicta exerts stabilizing selection to maintain spherical galls. In the forest there was directional selection for more spherical galls. Eurytoma gigantea exerted selection on gall shape in the forest in a complex manner that varied among years. We also supported the hypothesis that E. gigantea is coevolving with E. solidaginis. The parasitoid had significantly longer ovipositors in the prairie than in the forest, indicating the possibility that it has evolved in response to selection to reach larvae in the larger-diameter prairie galls.     

Phylogeography and the geographic cline in the armament of a seed-predatory weevil: effects of historical events vs. natural selection from the host plant

Japanese camellia (Camellia japonica) and its seed predator, the camellia weevil (Curculio camelliae), provide a notable example of a geographic mosaic of coevolution. In the species interaction, the offensive trait of the weevil (rostrum length) and the defensive trait of the plant (pericarp thickness) are involved in a geographically-structured arms race, and these traits and selective pressures acting on the plant defence vary greatly across a geographical landscape. To further explore the geographical structure of this interspecific interaction, we tested whether the geographical variation in the weevil rostrum over an 800-km range along latitude is attributed to local natural selection or constrained by historical (phylogeographical) events of local populations. Phylogeographical analyses of the mitochondrial DNA sequences of the camellia weevil revealed that this species has experienced differentiation into two regions, with a population bottleneck and subsequent range and/or population expansion within each region. Although these phylogeographical factors have affected the variation in rostrum length, analyses of competing factors for the geographical variation revealed that this pattern is primarily determined by the defensive trait of the host plant rather than by the effects of historical events of populations and a climatic factor (annual mean temperature). Thus, our study suggests the overwhelming strength of coevolutionary selection against the effect of historical events, which may have limited local adaptation.     

Arms races between social parasites and their hosts: geographic patterns of manipulation and resistance

The evolutionary interactions between permanently social parasiticspecies and their hosts are of special interest because socialparasites are not only closely dependent on, but are also closelyrelated to, their hosts. The small European slavemaker Harpagoxenussublaevis has evolved several characters that help manipulateits host. In this study we investigated adaptations of thissocial parasite to its local hosts and the geographic patternof host resistance in two main host species from three differentpopulations. In behavioral experiments, we examined whetherhost colonies from three geographically distant Leptothoraxacervorum populations varied in their ability to defend thenest against social parasites. Naive colonies from the unparasitizedEnglish population killed attacking slavemakers more often thandid host colonies from two parasitized populations. We alsofound strong interpopulation variation in the ability of theslavemaker to manipulate host behavior. H. sublaevis uses theDufour gland secretion to induce intracolonial fights and, ingeneral, this "propaganda" substance was most effective againstlocal hosts. Our results suggest that the social parasite isleading the arms race in this aspect. Similar experiments uncovereddifferences between two populations of the second host speciesL. muscorum and could demonstrate that nest defense in bothhost species is similarly efficient. In L. acervorum, monogynouscolonies were more successful in nest defense, whereas socialstructure had no impact in L. muscorum. Colony size did notaffect the efficacy of nest defense in either host species.The caste of the slavemaker had a strong influence on the successof an attack.     

A geographic mosaic of trophic interactions and selection: trees, aphids and birds

Genetic variation in plants is known to influence arthropod assemblages and species interactions. However, these influences may be contingent upon local environmental conditions. Here, we examine how plant genotype-based trophic interactions and patterns of natural selection change across environments. Studying the cottonwood tree, Populus angustifolia, the galling aphid, Pemphigus betae and its avian predators, we used three common gardens across an environmental gradient to examine the effects of plant genotype on gall abundance, gall size, aphid fecundity and predation rate on galls. Three patterns emerged: (i) plant genotype explained variation in gall abundance and predation, (ii) G×E explained variation in aphid fecundity, and environment explained variation in gall abundance and gall size, (iii) natural selection on gall size changed from directional to stabilizing across environments.     

Cuckoo parasitism and productivity in different magpie subpopulations predict frequencies of the 457bp allele: a mosaic of coevolution at a small geographic scale

The level of defense against great spotted cuckoo (Clamator glandarius) parasitism in different European populations of magpie (Pica pica) depends on selection pressures due to parasitism and gene flow between populations, which suggests the existence of coevolutionary hot spots within a European metapopulation. A mosaic of coevolution is theoretically possible at small geographical scales and with strong gene flow, because, among other reasons, plots may differ in productivity (i.e., reproductive success of hosts in the absence of parasitism) and defensive genotypes theoretically should be more common in plots of high productivity. Here, we tested this prediction by exploring the relationship between parasitism rate, level of defense against parasitism (estimated as both rejection rate and the frequency of the 457bp microsatellite allele associated with foreign egg rejection in magpies), and some variables related to the productivity (average laying date, clutch size, and number of hatchlings per nest) of magpies breeding in different subpopulations. We found that both estimates of defensive ability (egg rejection rate and frequency of the 457bp allele) covaried significantly with between-plot differences in probability of parasitism, laying date, and number of hatchlings per nest. Moreover, the parasitism rate was larger in more productive plots. These results confirm the existence of a mosaic of coevolution at a very local geographical scale, and the association between laying date and number of hatchlings with variables related to defensive ability and the selection pressure arising from parasitism supports the prediction of coevolutionary gradients in relation to host productivity.     

A role for habitat area in the geographic mosaic of coevolution between red crossbills and lodgepole pine

Understanding how resource abundance limits adaptive evolution and influences species interactions is an important step towards developing insight into the role of microevolutionary processes in establishing macroevolutionary patterns. We examined how variation in resource abundance (forest area of lodgepole pine Pinus contorta ssp. latifolia) influenced patterns of co-adaptation and coevolution between red crossbill (Loxia curvirostra complex) and lodgepole pine populations. First, we found that crossbill abundance increased logarithmically as forest area increased in mountain ranges lacking a preemptive competitor (pine squirrels Tamiasciurus hudsonicus). Second, seed defences against predation by crossbills increased with increases in crossbill density, suggesting that seed defences have likely evolved in proportion to the intensity of selection that crossbills exert. Third, the average bill size of crossbill populations increased with increasing seed defences, which implies that crossbill offenses increased with increases in seed defences. The large bill size on the largest range is the result of coevolution with lodgepole pine with this crossbill population perhaps speciating. Local adaptation of crossbill populations on smaller ranges, however, is more likely the result of resident crossbills representing a subset of the potential colonists (phenotypic sorting) than of local evolution. In the smallest range, migration and possibly more frequent extinction likely impede local adaptation and may result in maladaptation.     

Effects of melatonin on the behavioral and hormonal responses of red-sided garter snakes (Thamnophis sirtalis parietalis) to exogenous corticosterone

We investigated possible interactions between melatonin and corticosterone in modulating the reproductive behavior of male red-sided garter snakes (Thamnophis sirtalis parietalis) following spring emergence. We also examined whether melatonin's modulatory actions could be explained by its potential properties as a serotonin receptor antagonist. Exogenous corticosterone significantly reduced courtship behavior of male snakes in a dose-dependent manner. Melatonin also significantly reduced courtship behavior of male garter snakes. Pretreatment with melatonin before administering corticosterone treatments further suppressed courtship behavior of red-sided garter snakes. These results indicate additive inhibitory effects of melatonin and corticosterone in modulating reproductive behavior. Snakes receiving ketanserin, a serotonergic type 2A receptor antagonist, followed by corticosterone also showed reduced courtship behavior; this serotonin receptor antagonist followed by treatment with vehicle did not significantly influence courtship behavior of male snakes. Neither melatonin nor corticosterone treatments significantly influenced testosterone + 5-alpha-dihydrotestosterone concentrations of male garter snakes, supporting a direct effect of melatonin and corticosterone on courtship behavior that is independent of any effect on androgen concentrations. We propose that a serotonin system is involved in the modulation of male courtship behavior by melatonin and corticosterone. In addition, our data support the hypothesis that melatonin may function as a serotonin receptor antagonist. Further research is necessary to discern whether the actions of melatonin and corticosterone are converging on the same pathway or if their effects on different pathways are having additive inhibitory effects on courtship behavior.     

Bower-building: coevolution of display traits in response to the costs of female choice?

Bower-building is peculiar to polygynous species in the family Ptilonorhynchidae (Bowerbirds). Here we summarize past and current theories regarding the evolution of bower-building, evaluate the evidence that can be used to differentiate between them and suggest future areas for research.     

The evolution of novel herbicide tolerance in a noxious weed: the geographic mosaic of selection

Understanding how genetic variation is organized over geography has long been of interest to evolutionary biologists given that traits can vary within and among populations, across regions, and at continental or global scales. The pattern of regional variation can have an important impact on trait evolution at the local or population level. Using a common garden, we asked whether a geographically variable mosaic of tolerance to the widely applied herbicide RoundUp^® existed in two closely related co-occurring species of morning glory, Ipomoea purpurea and I. hederacea. We assayed RoundUp tolerance in over 1,700 plants representing 290 families from 29 populations in the southeastern United States. Our findings suggest that the two species of morning glory partition their respective levels of genetic variation for tolerance to glyphosate differently. Variation for tolerance in I. purpurea appears to exist among maternal lines and regions, whereas in I. hederacea, variation in tolerance existed only among populations. In addition, we find a significant hotspot of tolerance or positive spatial aggregation of this trait on a local scale in I. purpurea populations from the Coastal Plain. This suggests that either similar regimes of selection or gene flow between populations can produce a geographic mosaic of tolerance. These results highlight the fact that the genetic variation underlying an adaptive trait can exist at many different scales, whether it be within- or among-populations, among geographical ‘hotspots,’ or among distinct ecological regions. Given these results, the partitioning of genetic variation should be considered before making predictions about an adaptive trait’s evolutionary trajectory.     

How to fail in advertising: The potential of marketing theory to predict the community-level selection of defended prey

Economics and ecology both present us with a key challenge: scaling up from individual behaviour to community-level effects. As a result, biologists have frequently utilized theories and frameworks from economics in their attempt to better understand animal behaviour. In the study of predator–prey interactions, we face a particularly difficult task—understanding how predator choices and strategies will impact the ecology and evolution not just of individual prey species, but whole communities. However, a similar challenge has been encountered, and largely solved, in Marketing, which has created frameworks that successfully predict human consumer behaviour at the community level. We argue that by applying these frameworks to non-human consumers, we can leverage this predictive power to understand the behaviour of these key ecological actors in shaping the communities they act upon. We here use predator–prey interactions, as a case study, to demonstrate and discuss the potential of marketing and human-consumer theory in helping us bridge the gap from laboratory experiments to complex community dynamics.     

Spatial-temporal patterns in intra-annual gray whale foraging: Characterizing interactions between predators and prey in Clayquot Sound, British Columbia, Canada

In Clayquot Sound, British Columbia, gray whales (Eschrichtius robustus) forage primarily on mysids (Family Mysideae) and also on crab larvae (Family Porcellanidae) that are constrained to specific habitat, which relate to bathymetric depths. In this paper we characterize the interactions of gray whales and their prey by analyzing fine scale spatial‐temporal patterns in foraging gray whale distribution within a season. Kernel density estimators are applied to two seasons (1998 and 2002) of high‐resolution data on foraging by gray whales. By partitioning data from each foraging season into several time periods (12 in 1998 and 11 in 2002), using a temporal autocorrelation function, and generating kernel density estimated surfaces for each time period, it is possible to identify discrete areas of increasing and declining foraging effort. Our results indicate that gray whales forage on mysids throughout a season and opportunistically forage on crab larvae. The episodic crab larvae feeding may reduce, but not eliminate, pressure to mysid populations enabling mysids to reassemble swarms and continue to support gray whale foraging in the latter part of the season. Results suggest that when managing marine environments, gray whale populations require multiple and connected habitats for summer foraging.     

Evolution of prey behavior in response to changes in predation regime: damselflies in fish and dragonfly lakes

In a large behavioral experiment we reconstructed the evolution of behavioral responses to predators to explore how interactions with predators have shaped the evolution of their prey's behavior. All Enallagma damselfly species reduced both movement and feeding in the presence of coexisting predators. Some Enallagma species inhabit water bodies with both fish and dragonflies, and these species responded to the presence of both predators, whereas other Enallagma species inhabit water bodies that have only large dragonflies as predators, and these species only responded to the presence of dragonflies. Lineages that shifted to live with large dragonflies showed no evolution in behaviors expressed in the presence of dragonflies, but they evolved greater movement in the absence of predators and greater movement and feeding in the presence of fish. These results suggest that Enallagma species have evolutionarily lost the ability to recognize fish as a predator. Because species coexisting with only dragonfly predators have also evolved the ability to escape attacking dragonfly predators by swimming, the decreased predation risk associated with foraging appears to have shifted the balance of the foraging/predation risk trade-off to allow increased activity in the absence of mortality threats to evolve in these lineages. Our results suggest that evolution in response to changes in predation regime may have greater consequences for characters expressed in the absence of mortality threats because of how the balance between the conflicting demands of growth and predation risk are altered.     

The development of larval resistance to a nucleopolyhedrovirus is not accompanied by an increased virulence in the virus

Two laboratory experiments were conducted to examine the possible coevolution of cabbage loopers (Trichoplusia ni) and their S nucleopolyhedrovirus (TnSNPV). At the conclusion of Experiments 1 and 2, T. ni had respectively evolved 4.4 × and 22 × resistance to TnSNPV. The higher level of resistance achieved in Experiment 2 could be due to marginally stronger selection, possibly greater genetic variability in larval resistance to TnSNPV, or both. However, the evolution of resistance was not accompanied by an increased virulence of TnSNPV or a change in the restriction profile of the viral DNA when digested with BamHI, EcoRI, HindIII, PstI, SalI, SstI or XhoI. Little genetic variability for virulence in the initial TnSNPV stocks, low mutation rates and possibly weak selection on the virus are some factors that may have constrained the evolution of TnSNPV. We discuss our results in light of the geographic mosaic theory of coevolution and their implications for the use of TnSNPV as a biological control agent against T. ni. This revised version was published online in November 2006 with corrections to the Cover Date.     

Ecological and evolutionary components of body size: geographic variation of venomous snakes at the global scale

Biogeographical patterns of animal body size and the environmental and evolutionary mechanisms that may be driving them have been broadly investigated in macroecology, although just barely in ectotherms. We separately studied two snake clades, Viperidae and Elapidae, and used phylogenetic eigenvector regression and ordinary least squares multiple regression methods to perform a global grid-based analysis of the extent at which the patterns of body size (measured for each species as its log₁₀-transformed maximum body length) of these groups are phylogenetically structured or driven by current environment trends. Phylogenetic relatedness explained 20% of the across-species size variation in Viperidae, and 59% of that of Elapidae, which is a more recent clade. Conversely, when we analysed spatial trends in mean body size values (calculated for each grid-cell as the average size of its extant species), an environmental model including temperature, precipitation, primary productivity (as indicated by the global vegetation index) and topography (range in elevation) explained 37.6% of the variation of Viperidae, but only 4.5% of that of Elapidae. These contrasted responses of body size patterns to current environment gradients are discussed, taking into consideration the dissimilar evolutionary histories of these closely-related groups. Additionally, the results obtained emphasize the importance of the need to start adopting deconstructive approaches in macroecology.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 94–109.     

The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids

Abstract Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal trans-mission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts haveachieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont-conferredresistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show thatdefensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of thehost-parasitoid interaction, and by inducing environment-dependent trade-offs. These effects are conducive to very dynamic, symbiont-mediated coevolution that is driven by frequency-dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem byexploiting the parasitoids＇ demonstrated ability to rapidly evolve counteradaptations to symbiont-conferred resistance.     

The local introduction of strongly interacting species and the loss of geographic variation in species and species interactions

Species introductions into nearby communities may seem innocuous, however, these introductions, like long-distance introductions (e.g. trans- and intercontinental), can cause extinctions and alter the evolutionary trajectories of remaining community members. These 'local introductions' can also more cryptically homogenize formerly distinct populations within a species. We focus on several characteristics and the potential consequences of local introductions. First, local introductions are commonly successful because the species being introduced is compatible with existing abiotic and biotic conditions; many nearby communities differ because of historical factors and the absence of certain species is simply the result of barriers to dispersal. Moreover, the species with which they interact most strongly (e.g. prey) may have, for example, lost defences making the establishment even more likely. The loss or absence of defences is especially likely when the absent species is a strongly interacting species, which we argue often includes mammals in terrestrial communities. Second, the effects of the introduction may be difficult to detect because the community is likely to converge onto nearby communities that naturally have the introduced species (hence the perceived innocuousness). This homogenization of formerly distinct populations eliminates the geographic diversity of species interactions and the geographic potential for speciation, and reduces regional species diversity. We illustrate these ideas by focusing on the introduction of tree squirrels into formerly squirrel-less forest patches. Such introductions have eliminated incipient species of crossbills (Loxia spp.) co-evolving in arms races with conifers and will likely have considerable impacts on community structure and ecosystem processes.