Mosaic Theory Research Articles

Within-population genetic variability in mycorrhizal interactions

The geographic mosaic theory of coevolution hypothesizes that natural selection on species interactions varies among ecosystems, partly because the genes involved in species interactions differ in their fitness effects among environments. This selection mosaic may be expressed, at the extreme, as ecological outcomes ranging from mutualism to parasitism among environments. In a recent laboratory experiment on the interaction between a plant, bishop pine (Pinus muricata), and a root-symbiotic ectomycorrhizal fungus, Rhizopogon occidentalis, we demonstrated the potential for selection mosaics in that interaction, and the existence of substantial within-population genetic variation for symbiotic compatibility in the interaction. Here, we present the results from a second experiment on the interaction between the same ectomycorrhizal fungus and a different plant, shore pine (Pinus contorta var. contorta), designed to test for the presence of genetic variation for symbiotic compatibility in another similar system, and also to test whether such variation might be generated in part by adaptation of fungal lineages to individual trees. In this experiment, we found no genetic variation among plant lineages for compatibility with the fungal symbiont, and no evidence for adaptation of fungal lineages to individual plants, but the two fungal genotypes differed greatly in their compatibility with the plant hosts. Specifically, one of the two fungal genotypes not only colonized host plants less intensively than the other, but also had a negative effect on plant growth. Altogether, these results suggest the potential for ongoing natural selection on the ectomycorrhizal fungus, R. occidentalis, for different levels of symbiotic compatibility with particular pine hosts, but the mechanisms generating and maintaining genetic variation for symbiotic compatibility remain unclear. Such results will aid in efforts to develop realistic models of how plants and their symbionts coevolve over broad geographic ranges in which they co-occur.

Understanding the limits to generalizability of experimental evolutionary models

Given the difficulty of testing evolutionary and ecological theory in situ, in vitro model systems are attractive alternatives; however, can we appraise whether an experimental result is particular to the in vitro model, and, if so, characterize the systems likely to behave differently and understand why? Here we examine these issues using the relationship between phenotypic diversity and resource input in the T7-Escherichia coli co-evolving system as a case history. We establish a mathematical model of this interaction, framed as one instance of a super-class of host-parasite co-evolutionary models, and show that it captures experimental results. By tuning this model, we then ask how diversity as a function of resource input could behave for alternative co-evolving partners (for example, E. coli with lambda bacteriophages). In contrast to populations lacking bacteriophages, variation in diversity with differences in resources is always found for co-evolving populations, supporting the geographic mosaic theory of co-evolution. The form of this variation is not, however, universal. Details of infectivity are pivotal: in T7-E. coli with a modified gene-for-gene interaction, diversity is low at high resource input, whereas, for matching-allele interactions, maximal diversity is found at high resource input. A combination of in vitro systems and appropriately configured mathematical models is an effective means to isolate results particular to the in vitro system, to characterize systems likely to behave differently and to understand the biology underpinning those alternatives.

Natural history of Arabidopsis thaliana and oomycete symbioses

Molecular ecology of plant–microbe interactions has immediate significance for filling a gap in knowledge between the laboratory discipline of molecular biology and the largely theoretical discipline of evolutionary ecology. Somewhere in between lies conservation biology, aimed at protection of habitats and the diversity of species housed within them. A seemingly insignificant wildflower called Arabidopsis thaliana has an important contribution to make in this endeavour. It has already transformed botanical research with deepening understanding of molecular processes within the species and across the Plant Kingdom; and has begun to revolutionize plant breeding by providing an invaluable catalogue of gene sequences that can be used to design the most precise molecular markers attainable for marker-assisted selection of valued traits. This review describes how A. thaliana and two of its natural biotrophic parasites could be seminal as a model for exploring the biogeography and molecular ecology of plant–microbe interactions, and specifically, for testing hypotheses proposed from the geographic mosaic theory of co-evolution.

Natural variation in Pristionchus pacificus insect pheromone attraction involves the protein kinase EGL-4

The geographical mosaic theory of coevolution predicts that different local species interactions will shape population traits, but little is known about the molecular factors involved in mediating the specificity of these interactions. Pristionchus nematodes associate with different scarab beetles around the world, with Pristionchus pacificus isolated primarily from the oriental beetle in Japan. In particular, the constituent populations of P. pacificus represent a rare opportunity to study multiple specialized interactions and the mechanisms that influence population traits at the genetic level. We identified a component of the cGMP signaling pathway to be involved in the natural variation for sensing the insect pheromone ETDA, using targeted introgression lines, exogenous cGMP treatment, and a null egl-4 allele. Our data strongly implicate egl-4 as one of several loci involved in behavioral variation in P. pacificus populations. That EGL-4 homologs have been independently implicated for behavioral variations in other invertebrate models suggests that EGL-4 may act as a modulator for interspecies behavioral repertoires across large phylogenetic distances.

Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist

The interaction between Depressaria pastinacella (parsnip webworm) and wild parsnip (Pastinaca sativa), in its native Europe and in its longstanding nonindigenous range in the midwestern United States, is characterized by chemical phenotype matching, ostensibly mediated by reciprocal selective responses. The first appearance of D. pastinacella on P. sativa in New Zealand in 2004 provided an opportunity to quantify selective impacts of a coevolved herbivore and calibrate rates of phytochemical response in its host plant. Webworms in 2006 reduced seed production up to 75% in New Zealand populations, and in 2007 infestations increased in severity in all populations except one. Most New Zealand populations fall into a furanocoumarin phenotype cluster distinct from European and U.S. phenotypes, although one heavily attacked population clusters with two U.S. populations and one European population long associated with webworms. Multivariate selection analysis substituting realized fitness (with webworms present) for potential fitness (absent webworms) as the dependent variable revealed that reassociation with a coevolved specialist in a nonindigenous area profoundly altered the selection regime, favoring trait remixing and rapid chemical changes in parsnip populations, as predicted by the geographic mosaic theory. That uninfested populations of New Zealand parsnips contain higher amounts of octyl acetate, a floral volatile used by webworms for orientation, suggests that plants that escape from specialized enemies may also experience selection to increase kairomones, as well as to reduce allomones.

Les embryons d’ascidies

Ascidian embryos were the first animal embryos to be experimentally manipulated by Man at the end of the 19th century. The mosaic theory of development was born from these experiments and those carried out by Conklin 20 years later. These astonishing animals, some of which are eaten as delicacies in France and other countries, belong to the tunicates, which are the only animals to produce cellulose. They are, however, the closest living relatives to the vertebrates. Neglected throughout most of the 20th century, ascidians have recently come back in the limelight in the wake of the sequencing of the genomes of Ciona intestinalis and Ciona savignyi. These small, unduplicated genomes harbour 16,000 to 20,000 genes and are 20 times smaller than the human genome. Ciona eggs can be microinjected and easily electroporated, which make this system suitable for the study of developmental gene regulatory networks.

Increasing productivity accelerates host–parasite coevolution

Host-parasite coevolution is believed to influence a range of evolutionary and ecological processes, including population dynamics, evolution of diversity, sexual reproduction and parasite virulence. The impact of coevolution on these processes will depend on its rate, which is likely to be affected by the energy flowing through an ecosystem, or productivity. We addressed how productivity affected rates of coevolution during a coevolutionary arms race between experimental populations of bacteria and their parasitic viruses (phages). As hypothesized, the rate of coevolution between bacterial resistance and phage infectivity increased with increased productivity. This relationship can in part be explained by reduced competitiveness of resistant bacteria in low compared with high productivity environments, leading to weaker selection for resistance in the former. The data further suggest that variation in productivity can generate variation in selection for resistance across landscapes, a result that is crucial to the geographic mosaic theory of coevolution.

Process rather than pattern: finding pine needles in the coevolutionary haystack

The geographic mosaic theory is fast becoming a unifying framework for coevolutionary studies. A recent experimental study of interactions between pines and mycorrhizal fungi in BMC Biology is the first to rigorously test geographical selection mosaics, one of the cornerstones of the theory.

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.

Dos and don'ts of testing the geographic mosaic theory of coevolution

The geographic mosaic theory of coevolution is stimulating much new research on interspecific interactions. We provide a guide to the fundamental components of the theory, its processes and main predictions. Our primary objectives are to clarify misconceptions regarding the geographic mosaic theory of coevolution and to describe how empiricists can test the theory rigorously. In particular, we explain why confirming the three main predicted empirical patterns (spatial variation in traits mediating interactions among species, trait mismatching among interacting species and few species-level coevolved traits) does not provide unequivocal support for the theory. We suggest that strong empirical tests of the geographic mosaic theory of coevolution should focus on its underlying processes: coevolutionary hot and cold spots, selection mosaics and trait remixing. We describe these processes and discuss potential ways each can be tested.

POLYGENIC TRAITS AND PARASITE LOCAL ADAPTATION

The extent to which parasites are locally adapted to their hosts has important implications for human health and agriculture. A recently developed conceptual framework--the geographic mosaic theory of coevolution--predicts that local maladaptation should be common and largely determined by the interplay between gene flow and spatially variable reciprocal selection. Previous investigation of this theory has predominately focused on genetic systems of infection and resistance characterized by few genes of major effect and particular forms of epistasis. Here we extend existing theory by analyzing mathematical models of host-parasite interactions in which host resistance to parasites is mediated by quantitative traits with an additive polygenic basis. In contrast to previous theoretical studies predicated upon major gene mechanisms, we find that parasite local maladaptation is quite uncommon and restricted to one specific functional form of host resistance. Furthermore, our results show that local maladaptation should be rare or absent in studies that measure local adaptation using reciprocal transplant designs conducted in natural environments. Our results thus narrow the scope over which the predictions of the geographic mosaic theory are likely to hold and provide novel and readily testable predictions about when and where local maladaptation is expected.

Neotyphodium infection and hybridisation as a function of environmental variation

Neotyphodium is an asexual, vertically transmitted, obligate fungal endosymbiont infecting cool-season grasses such as Arizona fescue. The relationship between Neotyphodium and several native grass hosts ranges from antagonistic to mutualistic. One theory that may explain how Neotyphodium infection is maintained despite inconsistent mutualistic benefit to the host is the bounded hybrid superiority hypothesis. This hypothesis argues that hybrids are more fit than non-hybrids in response to some environmental stresses. Neotyphodium infects hosts in both hybrid and non-hybrid forms. We tested the possibility of hybrid superiority in depauperate habitats (low soil water and nitrate) by quantifying the types and frequency of host infections (uninfected, hybrid-infected and non-hybrid-infected), and the quality of resources available between three host populations. A second theory, the geographic mosaic theory of coevolution, may also explain different symbiotic outcomes at the population level in response to variation in abiotic and biotic population characters. We provide cursory support for both hypotheses. Keywords: geographic mosaic theory of coevolution, hybrid, Festuca, Neotyphodium, symbiosis, mutualism, bounded hybrid superiority

Regulator of G-Protein Signaling-2 as a Candidate Gene

The “mosaic theory” of hypertension has been the prevailing dogma since its enunciation more than a half century ago. However, the ongoing search has been to determine which of the myriad of alterations in blood pressure regulatory systems occurs earliest in the process and are critical in the maintenance of the hypertensive state. Much of that focus has been directed to the determinants of increased peripheral resistance—perhaps the hallmark of the hypertensive state. The mechanisms underlying this abnormality reflect a combination of both structural and functional factors. From a functional perspective, peripheral resistance reflects a net balance between vasoconstrictor and vasodilator mechanisms. Defects in vasodilator mechanisms and enhancement of vasoconstrictor mechanisms have been described in human hypertension as well as in animal models. Central among these mechanisms have been alterations in G-protein-coupled receptor (GPCR) signaling pathways. Alterations in GPCR-signaling pathways in the hypertensive state are probably best explained by alterations downstream from the receptor. For those GPCRs linked to Gs and adenylyl cyclase activation, the impairment in GPCR/ G-protein “coupling” reflects both decreased G-protein function as well as the impact of increased expression/activity of the G-protein receptor kinases that interdict GPCR/G-protein signaling.1 For those mechanisms linked to vasoconstrictor process (via either Gi or Gq) the alterations also appear to be generalized across a range of receptors, consistent with a “downstream” effect.2 For …

PARASITE LOCAL ADAPTATION IN A GEOGRAPHIC MOSAIC

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.

PARASITE LOCAL ADAPTATION IN A GEOGRAPHIC MOSAIC

A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.

Temporally persistent patterns of incidence and abundance in a pollinator guild at annual and decadal scales: the bees of Larrea tridentata

A recent alternative model to conventional coevolution, the geographic mosaic theory of coevolution, posits that reciprocal selection is episodic and local, rather than persistent and spatially extensive. However, little empirical evidence addresses this model's tenets, in particular the temporal stability of local plant–pollinator interactions. We evaluated this tenet using the richly diverse guild of bees at creosote bush (Larrea tridentata), a generalist plant that hosts many specialist bees. We systematically resampled over 2–5 years at 11 sites across the south-western USA. Incidence and abundance also were compared for survey sites sampled 20 ± 2 years earlier. Average Morisita-Horn faunal similarities of local bee guilds was 87% for sequential years and 36% after 20 years. Similarities in taxonomic composition of resampled local bee guilds could be statistically represented as a random assemblage drawn from the regional source pool of 54–68 bee species that could be expected at Larrea, weighted by regional abundance. At every site, only the minority of abundant bee species was typically persistent in local guilds, even after > 20 years. Most bee species in the Larrea guild were chronically uncommon, geographically sporadic and temporally unpredictable, attributes that render them numerically inconsequential as pollinators in their local guild. Persistence among abundant bee species in local pollinator assemblages satisfies one condition by which reciprocal selection could act locally. The well-being of these more abundant core species, and not bee diversity per se, may better characterize the health of such plant–pollinator associations. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 319–329.

Identification and distribution of protein families in 120 completed genomes using Gene3D

Using a new protocol, PFscape, we undertake a systematic identification of protein families and domain architectures in 120 complete genomes. PFscape clusters sequences into protein families using a Markov clustering algorithm (Enright et al., Nucleic Acids Res 2002;30:1575-1584) followed by complete linkage clustering according to sequence identity. Within each protein family, domains are recognized using a library of hidden Markov models comprising CATH structural and Pfam functional domains. Domain architectures are then determined using DomainFinder (Pearl et al., Protein Sci 2002;11:233-244) and the protein family and domain architecture data are amalgamated in the Gene3D database (Buchan et al., Genome Res 2002;12:503-514). Using Gene3D, we have investigated protein sequence space, the extent of structural annotation, and the distribution of different domain architectures in completed genomes from all kingdoms of life. As with earlier studies by other researchers, the distribution of domain families shows power-law behavior such that the largest 2,000 domain families can be mapped to approximately 70% of nonsingleton genome sequences; the remaining sequences are assigned to much smaller families. While approximately 50% of domain annotations within a genome are assigned to 219 universal domain families, a much smaller proportion (< 10%) of protein sequences are assigned to universal protein families. This supports the mosaic theory of evolution whereby domain duplication followed by domain shuffling gives rise to novel domain architectures that can expand the protein functional repertoire of an organism. Functional data (e.g. COG/KEGG/GO) integrated within Gene3D result in a comprehensive resource that is currently being used in structure genomics initiatives and can be accessed via http://www.biochem.ucl.ac.uk/bsm/cath/Gene3D/.

Adaptation varies through space and time in a coevolving host-parasitoid interaction.

One of the central challenges of evolutionary biology is to understand how coevolution organizes biodiversity over complex geographic landscapes. Most species are collections of genetically differentiated populations, and these populations have the potential to become adapted to their local environments in different ways. The geographic mosaic theory of coevolution incorporates this idea by proposing that spatial variation in natural selection and gene flow across a landscape can shape local coevolutionary dynamics. These effects may be particularly strong when populations differ across productivity gradients, where gene flow will often be asymmetric among populations. Conclusive empirical tests of this theory have been particularly difficult to perform because they require knowledge of patterns of gene flow, historical population relationships and local selection pressures. We have tested these predictions empirically using a model community of bacteria and bacteriophage (viral parasitoids of bacteria). We show that gene flow across a spatially structured landscape alters coevolution of parasitoids and their hosts and that the resulting patterns of adaptation can fluctuate in both space and time.

Material Issues: Dealing with Nonpublic Information

This article addresses the following key points: Information is considered material when the likelihood is high that a reasonable investor would consider it important to making an investment decision. In gray areas of materiality, an insider is best advised to forego a potentially profitable trade. The mosaic theory recognizes that analysts may combine publicly available information with nonmaterial, nonpublic information to produce an investment conclusion.

Bottom‐up control and co‐occurrence in complex communities: honeydew and nectar determine a rainforest ant mosaic

Complex distribution patterns of species‐rich insect communities in tropical rainforests have been intensively studied, and yet we know very little about processes that generate these patterns. We provide evidence for the key role of homopteran honeydew and plant nectar in structuring ant communities in an Australian tropical rainforest canopy and understorey. We also test the ant visitation of these resources against predictions derived from the ‘ant‐mosaic’ hypothesis. Two ant species were highly dominant in terms of territorial behaviour and abundance:OecophyllasmaragdinaandAnonychomyrma gilberti. Both dominant ant species monopolised large aggregations of honeydew‐producing homopterans. Attended homopteran species were highly segregated between these two ant species. For the use of extrafloral and floral nectar (involving 43 ant species on 48 plant species), partitioning of ant species among plant species and between canopy and understorey was also significant, but less pronounced. In contrast to trophobioses, simultaneous co‐occurrence of different nectar foraging ant species on the same plant individuals was frequent (23% of all surveys). While both dominant ant species were mutually exclusive on honeydew and nectar sources, co‐occurrence with non‐dominant ant species on nectaries was common. The proportion of visits with co‐occurrences was low for dominant ants and high for many sub‐ordinate species. These findings support the ant mosaic theory. The differential role of honeydew (as a specialised resource for dominant ants) and nectar (as an opportunistic resource for all ants including the co‐occurring non‐dominant species) provides a plausible structuring mechanism for the Australian canopy ant community studied.