Division of Environmental Biology

For a half century, habitat configuration – the arrangement of habitat patches within a landscape – has been central to theories of landscape ecology, population dynamics, and community assembly, in addition to conservation strategies. A recent hypothesis advanced by Fahrig (2013) would, if supported, greatly diminish the relevance of habitat configuration as a predictor of diversity. The Habitat Amount Hypothesis posits that the sample area effect overrides patch size and patch isolation effects of habitat fragmentation on species richness. It predicts that the amount of habitat in a local landscape, regardless of configuration, is the main landscape‐level determinant of species richness. If habitat amount is indeed the major, landscape‐level driver of species richness, the slopes of the species–area relationship (SAR) for otherwise similar fragmented and unfragmented landscapes should be indistinguishable. We tested the Habitat Amount Hypothesis with data from two replicated and controlled habitat fragmentation experiments that disentangle the effects of habitat amount and configuration. One experiment provided time‐series data on plant species richness and the other on micro‐arthropod species richness. We found that, relative to less fragmented habitats, the SARs for fragmented habitats have significantly higher slopes and that the magnitude of the difference in slopes increased over time. Relatively more species were lost in smaller areas when fragments were more isolated. In both experiments, the proportion of species lost due to increased habitat fragmentation was nearly identical to the proportion lost due to reduced habitat amount. Our results provide a direct and experimentally derived refutation of the Habitat Amount Hypothesis, supporting the long‐held view that in addition to area, patch isolation and configuration are important determinants of species richness. Differences in species richness between fragmented and non‐fragmented habitats increase over time, demonstrating that long‐term studies are needed to understand the effects of fragmentation, above and beyond the amount of habitat lost.

The phytochemical system of mustard-oil glucosides (glucosinolates) accompanied by the hydrolytic enzyme myrosinase (beta-thioglucosidase), the latter usually compartmented in special myrosin cells, characterizes plants in 16 families of angiosperms. Traditional classifications place these taxa in many separate orders and thus imply multiple convergences in the origin of this chemical defense system. DNA sequencing of the chloroplast rbcL gene for representatives of all 16 families and several putative relatives, with phylogenetic analyses by parsimony and maximum likelihood methods, demonstrated instead a single major clade of mustard-oil plants and one phylogenetic outlier. In a further independent test, DNA sequencing of the nuclear 18S ribosomal RNA gene for all these exemplars has yielded the same result, a major mustard-oil clade of 15 families (Akaniaceae, Bataceae, Brassicaceae, Bretschneideraceae, Capparaceae, Caricaceae, Gyrostemonaceae, Koeberliniaceae, Limnanthaceae, Moringaceae, Pentadiplandraceae, Resedaceae, Salvadoraceae, Tovariaceae, and Tropaeolaceae) and one outlier, the genus Drypetes, traditionally placed in Euphorbiaceae. Concatenating the two gene sequences (for a total of 3254 nucleotides) in a data set for 33 taxa, we obtain robust support for this finding of parallel origins of glucosinolate biosynthesis. From likely cyanogenic ancestors, the "mustard oil bomb" was invented twice.

Despite the apparent advantages of adaptive plasticity, it is not common. We examined the effects of variation and uncertainty on selection for plasticity using an individual-based computer simulation model. In the model, the environment consisted of a linear gradient of 50 demes with dispersal occurring either before or after selection. Individuals consisted of multiple loci whose phenotypic expression either are affected (plastic) or are not affected (nonplastic) by the environment. Typically, evolution occurred first as genetic differentiation, which was then replaced by the evolution of adaptive plasticity, opposite to the evolutionary trend that is often assumed. Increasing dispersal rates selected for plasticity, if selection occurred before dispersal. If selection occurred after dispersal, the highest plasticity was at intermediate dispersal rates. Temporal variation in the environment occurring after development, but before selection, favored the evolution of plasticity. With dispersal before selection, such temporal variation resulted in hyperplasticity, with a reaction norm much steeper than the optimum. This effect was enhanced with negative temporal autocorrelation and can be interpreted as representing a form of bet hedging. As the number of nonplastic loci increased, plasticity was disfavored due to an increase in the uncertainty of the genomic environment. This effect was reversed with temporal variation. Thus, variation and uncertainty affect whether or not plasticity is favored with different sources of variation-arising from the amount and timing of dispersal, from temporal variation, and even from the genetic architecture underlying the phenotype-having contrasting, interacting, and at times unexpected effects.

Adaptation to heterogeneous environments can occur via phenotypic plasticity, but how often this occurs is unknown. Reciprocal transplant studies provide a rich dataset to address this issue in plant populations because they allow for a determination of the prevalence of plastic versus canalized responses. From 31 reciprocal transplant studies, we quantified the frequency of five possible evolutionary patterns: (1) canalized response-no differentiation: no plasticity, the mean phenotypes of the populations are not different; (2) canalized response-population differentiation: no plasticity, the mean phenotypes of the populations are different; (3) perfect adaptive plasticity: plastic responses with similar reaction norms between populations; (4) adaptive plasticity: plastic responses with parallel, but not congruent reaction norms between populations; and (5) nonadaptive plasticity: plastic responses with differences in the slope of the reaction norms. The analysis included 362 records: 50.8% life-history traits, 43.6% morphological traits, and 5.5% physiological traits. Across all traits, 52% of the trait records were not plastic, and either showed no difference in means across sites (17%) or differed among sites (83%). Among the 48% of trait records that showed some sort of plasticity, 49.4% showed perfect adaptive plasticity, 19.5% adaptive plasticity, and 31% nonadaptive plasticity. These results suggest that canalized responses are more common than adaptive plasticity as an evolutionary response to environmental heterogeneity.

Although boron has a relatively low natural abundance, it is an essential plant micronutrient. Boron deficiencies cause major crop losses in several areas of the world, affecting reproduction and yield in diverse plant species. Despite the importance of boron in crop productivity, surprisingly little is known about its effects on developing reproductive organs. We isolated a maize (Zea mays) mutant, called rotten ear (rte), that shows distinct defects in vegetative and reproductive development, eventually causing widespread sterility in its inflorescences, the tassel and the ear. Positional cloning revealed that rte encodes a membrane-localized boron efflux transporter, co-orthologous to the Arabidopsis thaliana BOR1 protein. Depending on the availability of boron in the soil, rte plants show a wide range of phenotypic defects that can be fully rescued by supplementing the soil with exogenous boric acid, indicating that rte is crucial for boron transport into aerial tissues. rte is expressed in cells surrounding the xylem in both vegetative and reproductive tissues and is required for meristem activity and organ development. We show that low boron supply to the inflorescences results in widespread defects in cell and cell wall integrity, highlighting the structural importance of boron in the formation of fully fertile reproductive organs.

Although adaptive plasticity would seem always to be favored by selection, it occurs less often than expected. This lack of ubiquity suggests that there must be trade-offs, costs, or limitations associated with plasticity. Yet, few costs have been found. We explore one type of limitation, a correlation between plasticity and developmental instability, and use quantitative genetic theory to show why one should expect a genetic correlation. We test that hypothesis using the Landsberg erecta × Cape Verde Islands recombinant inbred lines (RILs) of Arabidopsis thaliana. RILs were grown at four different nitrogen (N) supply levels that span the range of N availabilities previously documented in North American field populations. We found a significant multivariate relationship between the cross-environment trait plasticity and the within-environment, within-RIL developmental instability across 13 traits. This genetic covariation between plasticity and developmental instability has two costs. First, theory predicts diminished fitness for highly plastic lines under stabilizing selection, because their developmental instability and variance around the optimum phenotype will be greater compared to nonplastic genotypes. Second, empirically the most plastic traits exhibited heritabilities reduced by 57% on average compared to nonplastic traits. This demonstration of potential costs in inclusive fitness and heritability provoke a rethinking of the evolutionary role of plasticity.

A scientific field matures as its theoretical underpinnings consolidate around unified theories: conceptual structures consisting of a few general propositions that encompass a wide domain of phenomena and from which can be derived an array of models. We demonstrate this process with a synthetic theory of ecological gradients and species richness. Our unified theory rests on four propositions. First, variation in some environmental factor effects variation in the number of individuals creating a gradient. Second, in a uniform environment of fixed area, more individuals lead to more species. Third, the variance of an environmental factor increases with its mean for sites of equal area. Fourth, all nonmonotonic relationships (i.e., hump shaped or U shaped) require a trade-off in organismal performance or in population characteristics with respect to the environmental gradient. We identify 17 models that link environmental gradients with diversity, show their relationship to our framework, and describe issues surrounding their empirical testing. We illustrate how a general theory can be used to build new models such as that for the U-shaped productivity-diversity relationship. Finally, we discuss how our theory could be unified further with other theories of diversity and indicate other areas of ecology that are ripe for unification. By providing an example of the process of theory unification, we hope to encourage such efforts throughout ecology.

Science progresses faster when researchers operate within an explicit framework of concepts and theories, but currently biology has no explicit, overarching conceptual framework and few general theories. The single general theory currently recognized is that of evolution, which was put forth by Charles Darwin 150 years ago. Recently, Scheiner and Willig (2008) explicated a similarly general theory of ecology. In this paper, using the theory of evolution as an exemplar, I discuss the nature of theory in biology and put forth an overarching theory, as well as new general theories for cells, organisms, and genetics. Along with the theories of evolution and ecology, these constitute a general conceptual framework for the biological sciences. This framework reveals linkages among the various parts of biology, makes explicit the assumptions behind more narrow theories and models, and provides new insights into the structures of biological theories. This framework can also be used as a teaching tool, moving the teaching of biology beyond the transference of a vast compendium of facts. My hope is that this essay will lead to a vigorous discussion and debate across all of biology about the nature and structure of its theories.

Summary Understanding changes of biodiversity across the landscape underlies biogeography and ecology and is important in land management and conservation. Measures of species and phylogenetic turnover used to estimate the rate of change of assemblages between sets of locations are more often influenced by wide‐ranging taxa. Transition zones between regions that are associated with range‐restricted taxa can be obscured by wide‐ranging taxa that span them. We present a set of new range‐weighted metrics of taxon and phylogenetic turnover, as modifications of conventional metrics, where the range‐restricted components of the assemblages are assigned greater weight in the calculations. We show how these metrics are derived from weighted endemism and phylogenetic endemism and demonstrate their properties using a continent‐wide data set of Australian Acacia . The range‐weighted metrics result in better delineated transition zones between regions, in that the rate of turnover is steeper than with conventional turnover measures. These metrics provide important complementary information for the interpretation of spatial turnover patterns derived from conventional turnover metrics. Additionally, the phylogenetic variant incorporates information about phylogenetic relatedness while also not saturating at high values of turnover, thus remaining useful for comparisons over greater distances than conventional turnover metrics.

We examined the effect of agricultural land use on whole‐stream nutrient availability, biofilm standing crop, and biofilm nutrient limitation and uptake in 21 stream locations in southeastern Idaho. Higher stream water concentrations of dissolved organic carbon (DOC), but not nitrate (NO 3 ‐N) or phosphate (PO 4 ‐P), were associated with % agriculture in the watershed. Streambed chlorophyll a (Chl a ) and ash free dry weight (AF dry wt) also increased with agricultural land use. Nutrient diffusing substrate (NDS) bioassays, which determine biofilm nutrient limitation, showed that Chl a was NO 3 ‐N limited and suppressed by labile DOC, whereas AF dry wt did not respond to either NO 3 ‐N or labile DOC additions. Together, the different responses of Chl a and AF dry wt suggest potential competition between biofilm autotrophs and heterotrophs for nutrients or other resources. Nutrient uptake, determined with short‐term releases of NO 3 ‐N, PO 4 ‐P, and DOC (as glucose) showed that NO 3 ‐N uptake velocity (V f ) increased with agricultural land use. Despite the N‐limited status of biofilms indicated by the NDS results, uptake of NO 3 ‐N could not be consistently detected at all locations. The differences in response of biofilm to organic carbon enrichment suggests a difference in DOC quality, with labile DOC added with NDS compared to perhaps less‐labile DOC found in‐stream. Linking the interactive responses of biofilm communities to altered nutrient availability is an important step toward understanding whole ecosystem responses to land‐use change.

The core-periphery hypothesis (CPH) predicts that populations located at the periphery of a species' range should have lower levels of genetic variation than those at the centre of the range. However, most of the research on the CPH focuses on geographic distance and not on ecological distance, or uses categorical definitions of core and periphery to explain the distribution of genetic diversity. We use current climate data and historical climate data from the last glacial maxima to develop quantitative estimates of contemporary and historical ecological suitability using ecological niche models. We analysed genetic diversity using 12 polymorphic microsatellites to estimate changes in heterozygosity, allelic richness and population differentiation in 31 populations of the wood frog (Lithobates sylvaticus) spanning the species' entire eastern clade (33(o) to 45(o) latitude) from Alabama, USA, to Nova Scotia, Canada. Our data support predictions based on the CPH. Populations showed significant differences in genetic diversity across the range, with lower levels of genetic variation at the geographic range edge and in areas with lower levels of historical and contemporary ecological suitability. However, history and geography (not current ecological suitability) best explain the patterns. This study highlights the importance of examining more than just geography when assessing the CPH, and the importance of historical ecological suitability in the maintenance of genetic diversity and population differentiation.

Confronted with variable environments, species adapt in several ways, including genetic differentiation, a jack-of-all-trades strategy, or phenotypic plasticity. Adaptive habitat choice favors genetic differentiation and local adaptation over a generalist, jack-of-all-trades strategy. Models predict that, absent plasticity costs, variable environments generally favor phenotypic plasticity over genetic differentiation and being a jack-of-all-trades generalist. It is unknown how habitat choice might affect the evolution of plasticity. Using an individual-based simulation model, I explored the interaction of choice and plasticity. With only spatial variation, habitat choice promotes genetic differentiation over a jack-of-all-trades strategy or phenotypic plasticity. In the absence of plasticity, temporal variation favors a jack-of-all-trades strategy over choice-mediated genetic differentiation; when plasticity is an option, it is favored. This occurs because habitat choice creates a feedback between genetic differentiation and dispersal rates. As demes become better adapted to their local environments, the effective dispersal rate decreases, because more individuals have very high fitness and so choose not to disperse, reinforcing local stabilizing selection and negating selection for plasticity. Temporal variation breaks that feedback. These results point to a potential data paradox: systems with habitat choice may have the lowest actual movement rates. The potential for adaptive habitat choice may be very common, but its existence may reduce observed dispersal rates enough that we do not recognize systems where it may be present, warranting further exploration of likely systems.

In a heterogeneous environment, natural selection on a trait can lead to a variety of outcomes, including phenotypic plasticity and bet-hedging through developmental instability. These outcomes depend on the magnitude and pattern of that heterogeneity and the spatial and temporal distribution of individuals. However, we do not know if and how those two outcomes might interact with each other. I examined the joint evolution of plasticity and instability through the use of an individual-based simulation in which each could be genetically independent or pleiotropically linked. When plasticity and instability were determined by different loci, the only effect on the evolution of plasticity was the elimination of plasticity as a bet-hedging strategy. In contrast, the effects on the evolution of instability were more substantial. If conditions were such that the population was likely to evolve to the optimal reaction norm, then instability was disfavored. Instability was favored only when the lack of a reliable environmental cue disfavored plasticity. When plasticity and instability were determined by the same loci, instability acted as a strong limitation on the evolution of plasticity. Under some conditions, selection for instability resulted in maladaptive plasticity. Therefore, before testing any models of plasticity or instability evolution, or interpreting empirical patterns, it is important to know the ecological, life history, developmental, and genetic contexts of trait phenotypic plasticity and developmental instability.

Understanding regional carbon budgets is a leading issue in carbon cycling research, but issues of measurement difficulty, scale, boundaries, and logistics compromise estimates at areas larger than stands or research plots. We studied four 15 × 15 km sample areas to examine land management and wildfire effects on carbon storage dynamics in the forested southeastern U.S. coastal plain region from 1975 to 2001. Carbon exchange and storage rates were estimated using satellite remote‐sensing methods coupled with micrometeorological and biomass measurements. Carbon losses occurred by timber harvesting and fire, and carbon release continued for four years following clearing, suppressing landscape carbon gain proportional to the cleared area. Carbon accumulated at an average rate of 90,000 t C yr −1 in the landscape (total area 900 km 2 ) from 1975–2000, or ∼1 t C ha −1 yr −1 . Interannual variation was related mainly to the magnitude of annual plantation timber harvesting. Wildfires were rare and their effects on carbon balances consequently small, despite having large local impact. Previous studies in the area demonstrated that environmental fluctuations had little direct effect on the net landscape exchange of carbon, although indirect effects included higher probability of fire during droughts and shifts in harvesting to drier sites during wet periods. Although this study was a simple aggregation of carbon cycle components from fine spatial scale (Landsat images) to the landscape, the extrapolation incorporated important spatial and temporal environmental heterogeneities and led to the unexpected suggestion that the industrial forests of the southeast U.S. Coastal plain are a long‐term carbon sink. The analysis also revealed specific uncertainties in our scaling efforts that point to future research needs.

One potential evolutionary response to environmental heterogeneity is the production of randomly variable offspring through developmental instability, a type of bet-hedging. I used an individual-based, genetically explicit model to examine the evolution of developmental instability. The model considered both temporal and spatial heterogeneity alone and in combination, the effect of migration pattern (stepping stone vs. island), and life-history strategy. I confirmed that temporal heterogeneity alone requires a threshold amount of variation to select for a substantial amount of developmental instability. For spatial heterogeneity only, the response to selection on developmental instability depended on the life-history strategy and the form and pattern of dispersal with the greatest response for island migration when selection occurred before dispersal. Both spatial and temporal variation alone select for similar amounts of instability, but in combination resulted in substantially more instability than either alone. Local adaptation traded off against bet-hedging, but not in a simple linear fashion. I found higher-order interactions between life-history patterns, dispersal rates, dispersal patterns, and environmental heterogeneity that are not explainable by simple intuition. We need additional modeling efforts to understand these interactions and empirical tests that explicitly account for all of these factors.

Identifying geographical areas with the greatest representation of the tree of life is an important goal for the management and conservation of biodiversity. While there are methods available for using a single phylogenetic tree to assess spatial patterns of biodiversity, there has been limited exploration of how separate phylogenies from multiple taxonomic groups can be used jointly to map diversity and endemism. Here, we demonstrate how to apply different phylogenetic approaches to assess biodiversity across multiple taxonomic groups. We map spatial patterns of phylogenetic diversity/endemism to identify concordant areas with the greatest representation of biodiversity across multiple taxa and demonstrate the approach by applying it to the Murray-Darling basin region of southeastern Australia. The areas with significant centers of phylogenetic diversity and endemism were distributed differently for the five taxonomic groups studied (plant genera, fish, tree frogs, acacias, and eucalypts); no strong shared patterns across all five groups emerged. However, congruence was apparent between some groups in some parts of the basin. The northern region of the basin emerges from the analysis as a priority area for future conservation initiatives focused on eucalypts and tree frogs. The southern region is particularly important for conservation of the evolutionary heritage of plants and fishes.

Despite experimental and observational studies demonstrating that biodiversity enhances primary productivity, the best metric for predicting productivity at broad geographic extents-functional trait diversity, phylogenetic diversity, or species richness-remains unknown. Using >1.8 million tree measurements from across eastern US forests, we quantified relationships among functional trait diversity, phylogenetic diversity, species richness, and productivity. Surprisingly, functional trait and phylogenetic diversity explained little variation in productivity that could not be explained by tree species richness. This result was consistent across the entire eastern United States, within ecoprovinces, and within data subsets that controlled for biomass or stand age. Metrics of functional trait and phylogenetic diversity that were independent of species richness were negatively correlated with productivity. This last result suggests that processes that determine species sorting and packing are likely important for the relationships between productivity and biodiversity. This result also demonstrates the potential confusion that can arise when interdependencies among different diversity metrics are ignored. Our findings show the value of species richness as a predictive tool and highlight gaps in knowledge about linkages between functional diversity and ecosystem functioning.

Habitat fragmentation affects species and their interactions through intertwined mechanisms that include changes to fragment area, shape, connectivity and distance to edge. Disentangling these pathways is a fundamental challenge of landscape ecology and will help identify ecological processes important for management of rare species or restoration of fragmented habitats. In a landscape experiment that manipulated connectivity, fragment shape, and distance to edge while holding fragment area constant, we examined how fragmentation impacts herbivory and growth of nine plant species in longleaf pine savanna. Probability of herbivory in open habitat was strongly dependent on proximity to forest edge for every species, increasing with distance to edge in six species (primarily grasses and annual forbs) and decreasing in three species (perennial forbs and a shrub). In the two species of perennial forbs, these edge effects were dependent on fragment shape; herbivory strongly decreased with distance to edge in fragments of two shapes, but not in a third shape. For most species, however, probability of herbivory was unrelated to connectivity or fragment shape. Growth was generally determined more strongly by leaf herbivory than by distance to edge, fragment shape, or connectivity. Taken together, these results demonstrate consistently strong edge effects on herbivory, one of the most important biotic factors determining plant growth and demography. Our results contrast with the generally inconsistent results of observational studies, likely because our experimental approach enabled us to tease apart landscape processes that are typically confounded.

The ecological and evolutionary factors that drive the emergence and maintenance of variation in mutualistic benefit (i.e., the benefits provided by one partner to another) in mutualistic symbioses are not well understood. In this study, we evaluated the role that host and symbiont phylogeny might play in determining patterns of mutualistic benefit for interactions among nine species of Acacia and 31 strains of nitrogen-fixing rhizobial bacteria. Using phylogenetic comparative methods we compared patterns of variation in mutualistic benefit (host response to inoculation) to rhizobial phylogenies constructed from housekeeping and symbiosis genes; and a multigene host phylogeny. We found widespread genotype-by-genotype variation in patterns of plant growth. A relatively large component of this variation (21-28%) was strongly influenced by the interacting evolutionary histories of both partners, such that phylogenetically similar host species had similar growth responses when inoculated with phylogenetically similar rhizobia. We also found a relatively large nonphylogenetic effect for the average mutualistic benefit provided by rhizobia to plants, such that phylogenetic relatedness did not predict the overall benefit provided by rhizobia across all hosts. We conclude that phylogenetic relatedness should frequently predict patterns of mutualistic benefit in acacia-rhizobial mutualistic interactions; but that some mutualistic traits also evolve independently of the phylogenies.

Plastic changes in organisms' phenotypes can result from either abiotic or biotic effectors. Biotic effectors create the potential for a coevolutionary dynamic. Through the use of individual-based simulations, we examined the coevolutionary dynamic of two species that are phenotypically plastic. We explored two modes of biotic and abiotic interactions: ecological interactions that determine the form of natural selection and developmental interactions that determine phenotypes. Overall, coevolution had a larger effect on the evolution of phenotypic plasticity than plasticity had on the outcome of coevolution. Effects on the evolution of plasticity were greater when the fitness-maximizing coevolutionary outcomes were antagonistic between the species pair (predator-prey interactions) than when those outcomes were augmenting (competitive or mutualistic). Overall, evolution in the context of biotic interactions reduced selection for plasticity even when trait development was responding to just the abiotic environment. Thus, the evolution of phenotypic plasticity must always be interpreted in the full context of a species' ecology. Our results show how the merging of two theory domains--coevolution and phenotypic plasticity--can deepen our understanding of both and point to new empirical research.