January American Naturalist highlights

January 04, 2008

"Experimental evidence that selection favors character displacement in the ivyleaf morning glory"
Robin Ann Smith and Mark D. Rausher (Duke University)

How do we know that interactions between plant species affect their evolution" While there is abundant evidence to suggest that plant-pollinator interactions influence the evolution of floral traits, there is little direct evidence that interactions between plant species shape the evolution of such characteristics. Evolutionary biologists Robin Smith and Mark Rausher of Duke University recently examined this question in a study of two morning glory species that commonly co-occur in the southeastern United States. By measuring patterns of selection on floral traits of the focal species (the ivyleaf morning glory) in the presence and absence of flowers of a second species (the tall morning glory), they found direct experimental evidence that reproductive interference between closely related plant species can alter patterns of selection on floral traits that influence the mating system and contribute to reproductive isolation.

In the summer of 2004, Robin Smith and Mark Rausher conducted a field experiment in which they planted over 1,350 morning glories (~650 individuals of each species) checkerboard fashion in an abandoned agricultural field in central North Carolina. Using hand-sewn bags made of bridal veil mesh to cover the plants and control whether pollinators could transfer pollen between the two species, their aim was to determine whether reproductive interference from the tall morning glory alters the pattern of selection on floral traits of the ivyleaf morning glory. "The advantage of this experimental design is that it allowed us to manipulate only one variable--the presence vs. absence of flowers of the second species--while keeping all other environmental conditions constant," says Robin Smith, the study's lead author. They found that selection acts to increase clustering of anthers and stigma (the parts of a flower that send and receive pollen) when flowers of the second species are present. "Since clustering of anthers and stigma is known to promote self-fertilization, this suggests that one way for plants to avoid pollen deposition from the wrong species is to increase the rate of self-pollination," says Robin Smith. "In a broader sense, however, these results are important because they provide direct evidence for what ecological and evolutionary theory has long predicted, which is that species interactions can influence selection on morphological traits and drive phenotypic divergence."

"Genetic constraints and the evolution of display trait sexual dimorphism by natural and sexual selection"
Stephen F. Chenoweth (University of Queensland), Howard D. Rundle (University of Queensland and University of Ottawa), and Mark W. Blows (University of Queensland)

Same, but different: the evolution of male-female differences within a shared genome

One of the major components of the world's biological diversity are the differences between males and females in traits related to mating, including weapons used when competing for mates and display traits used to seduce them. Such gender differences are thought to arise because selection acts differently on each sex. The conflicting interests of males and females in reproduction are thought to be a key source of sex-specific selection on such traits. The evolution of sexual dimorphism is hampered, however, because the sexes share the majority of their genomes; an adaptive response to selection in one sex may therefore cause nonadaptive changes in the other as a correlated response. In a recent study, Steve Chenoweth and colleagues Howard Rundle and Mark Blows from the University of Queensland, Australia, tackle the combined issues of genetic control and sex-specific selection in a comprehensive investigation of the evolution of male-female differences in a set of sexual display traits in the Australian fruit fly, Drosophila serrata.

Both male and female Drosophila serrata use a set of pheromonal displays during mating, but differ in the relative concentrations of the individual compounds. Using a series of natural populations collected across a wide latitudinal gradient along the east coast of Australia, the authors show that the amount of sexual dimorphism varies and that these differences among populations are genetic. Using classic quantitative genetic methods, they demonstrate that the relaxation of genetic constraints appears to have occurred largely via genes on the X chromosome. "There are a number of mechanisms by which genetic constraints can be overcome," says Dr. Steve Chenoweth, "Our results suggest that sex-linkage may be key." By manipulating both natural and sexual selection and observing the evolutionary response in the laboratory, the authors also show that, as expected, sexual selection appears to generate sex-specific optima for these pheromones. Contrary to expectation, however, females and not males responded to sexual selection. "This suggests that the classic scenario of males as the sole target of sexual selection may be overly simplistic," states Dr. Howard Rundle. "If you want to know why males and females differ, you need to consider all forms of selection on both sexes."

"Multifunctional bracts in the dove tree Davidia involucrata (Nyssaceae: Cornales): rain protection and pollinator attraction"
Ji-Fan Sun (Wuhan University), Yan-Bing Gong (Wuhan University), Susanne S. Renner (University of Munich), and Shuang-Quan Huang (Wuhan University)

Davidia involucrata, the handkerchief tree or dove tree, is widely cultivated in parks and gardens because of its striking white bracts, which can reach 50 square cm in size. What might be the function of these bracts" This question had never been investigated, partly perhaps because in its native habitat in subtropical western China the tree flowers during the rainy season. To find out the bracts' function, scientists at Wuhan University in China observed pollinators and seed set in natural and manipulated flower heads that had their bracts removed or replaced by white or green paper. Davidia flowers are tiny and have no petals; their sole reward is pollen, which is offered over several days and collected by many species of bees. Experimental immersion of pollen grains in water resulted in rapid loss of viability, and flower heads that had their bracts removed lost a lot of pollen to rain. Together with the pollinating bees' preference for white-bracted flower heads, these findings suggest that the huge bracts serve as a rain umbrella as well as a pollinator signal. Rain is a surprisingly understudied selective factor on flowers, especially as regards its effects on pollen viability. The results of this study also highlight the difficulty of experimentally dissecting a structure's multipurpose function.

"Extending nonlinear analysis to short ecological time series"
Chih-hao Hsieh, Christian Anderson, and George Sugihara (University of California, San Diego)

Animal populations and the stock market are hard to forecast. Both are generated by complicated, interdependent systems. Unlike financial stocks, where trades are meticulously recorded, scientists began estimating animal populations only a few decades ago. But a new technique makes it possible to use the same tools some banks use to forecast the stock market and apply them to ecology. The newly developed "Dewdrop Regression" can forecast fish populations with 3% the data previously required through other methods, according to Hsieh, Anderson, and Sugihara in an article appearing in The American Naturalist.

The migration of the forecast tools from finance to ecology parallels Dr. Sugihara's own journey. After proposing simplex projection in 1990 with Lord Robert May, later Chief Science Advisor of the UK and President of the Royal Society, Sugihara became a managing director of a major bank for several years. Returning to academia and ecology, "I realized that even great ecologists were working with time series only a few tens of points long," Sugihara said. To apply data-hungry techniques to short time series, Hsieh et al. take data from several species collected simultaneously over a few years and stitch them together. A few test manipulations need to be applied; but when done properly, the technique is able to forecast with 15-20 points instead of 1,000. "You're doing significantly better than chance within four years," said Anderson.

But does it work for real world ecological problems" Using 40-year time series from 23 California fish species, Hsieh et al. showed that though they were <10% predictable alone, they become >60% predictable with the new procedure, combined with others from the same habitat. "When you consider that we're predicting the change, not just raw abundance, this accuracy becomes very exciting," Anderson said.

"What makes a host profitable" parasites balance host nutritive resources against immunity"
Pierre Bize (Glasgow University), Caroline Jeanneret (University of Lausanne), Aurélie Klopfenstein (University of Lausanne), and Alexandre Roulin (University of Lausanne)

Is host immunity enough to explain parasite success" Scientists based at the Universities of Glasgow, Scotland, and Lausanne, Switzerland, have shown that parasites balance host nutritive resources against immunity. Pierre Bize, Caroline Jeanneret, Aurélie Klopfenstein, and Alexandre Roulin conducted research in Switzerland in a free-living colonial bird whose nestlings are heavily infested by blood sucking ectoparasites. They observed that ectoparasites achieved highest survival on nestlings in intermediate condition. By manipulating nestling food resources and cutaneous immune responses, they then demonstrated that ectoparasite blood meal size, and in turn survival, is shaped positively by host nutritive resources and negatively by host immunity. "The important point of our study," states Pierre Bize, the lead author, "is that although parasites have a poor survival when feeding on hosts in prime conditions, because these hosts can mount a potent immune response, the reverse is not true. Indeed, parasites also have a reduced survival when feeding on hosts in poor conditions and with a low immune response, which points out that immunity is not the only factor accounting for parasite fitness." Alexandre Roulin adds, "The appraisal of what factors make a host profitable are vital for our understanding of host-parasite interactions, and in turn to the implement of well-designed parasite control programmes."

"Linking traits to energetics and population dynamics to predict lizard ranges in changing environments"
Lauren B. Buckley (Santa Fe Institute)

Does biology matter when predicting how animals will respond to climate change"

Most predictions of how animals will move in changing climates rely on statistically relating an animal's current location to environmental conditions. This approach ignores potentially important aspects of an animal's biology including size, physiology, and behavior. Lauren Buckley, an ecologist at the Santa Fe Institute, has developed a bottom-up approach that predicts distributions directly from an animal's traits and environmental conditions by modeling the energy use of individuals and populations. Research forthcoming in The American Naturalist applies the model to five populations of a widespread North American lizard, Sceloporus undulatus, to examine whether geographic variation in traits influences range predictions. Buckley finds that lizards from the five populations are suited to live in different areas and are predicted to respond differently to a climate warming of 3°C, contrasting the predictions of statistical models. While all populations are predicted to shift northward in response to climate warming, the extent of the predicted northward shift depends on the lizard's traits.

The research suggests that mechanistic modeling approaches that consider an animal's biology will be essential to realistic predictions of how animals will respond to climate change. The research points to the importance of biological factors such as adaptation of physiology, interactions with other organisms, and movement limitations. "Additional biologically-based approaches to predicting how animals will respond to climate change are urgently needed," noted Buckley. "Without such approaches, we will likely be surprised by how the peculiarities of an animal's biology influence its range shifts."

"Increased lifespan in a polyphenic butterfly artificially selected for starvation resistance"
Jeroen Pijpe, Paul M. Brakefield, and Bas J. Zwaan (Leiden University)

Why do some live longer than others?

In a recent article in The American Naturalist, researchers from Leiden University, the Netherlands, turned to tropical African butterflies to find the answer. "The definitive answer is still not known, but our results give an interesting new insight into the evolution of lifespan," says Jeroen Pijpe, first author of the paper.

He and his colleagues used what is called artificial selection to create genetically long-lived butterflies of the species Bicyclus anynana. "Basically, we use what the species does naturally, and magnify the bit we're interested in here in the lab in Leiden." In the field, the temperature experienced by the caterpillar sets up the butterfly to become the form that matches the season. This is called phenotypic plasticity, and in this species it has evolved as a response to the alternating seasons. The dry season form is long-lived and more starvation resistant. In the wet season, reproduction takes place. In this case, the authors selected on starvation resistance under wet-seasonal conditions.

They discovered that female butterflies had shifted their reproduction from quantity to quality of offspring. Next, they found that males and females had responded differently to the artificial selection: males seemed to have lowered their energy consumption, whilst females had increased the amount of energy to spend. "Both results offer interesting details not found previously in comparable experiments using fruit flies," Pijpe states. However, the most important finding was that the artificial selection in a wet seasonal environment had produced butterflies that resembles the long-lived dry season form. Pijpe says: "In other words, we targeted genes that are needed to live longer, and the result is very much like how temperature induces butterflies to live longer in the dry season." It suggests that, in this species, the evolution of lifespan is closely associated with phenotypic plasticity. Is it a general mechanism" "We think it is likely that the regulation of lifespan involves mechanisms of phenotypic plasticity during development, also in humans."

"An analytically tractable model for competitive speciation"
Pleuni S. Pennings (Ludwig-Maximilians University), Michael Kopp (Ludwig-Maximilians University), Geza Meszena (Eotvos University), Ulf Dieckmann (International Institute for Applied Systems Analysis), and Joachim Hermisson (Ludwig-Maximilians University)

Under which circumstances is sympatric speciation possible" An answer to this long-standing question of evolutionary biology has turned out to be challenging. In particular, models for the evolution of assortative mating under frequency-dependent disruptive selection necessarily depend on a large number of ecological and genetic factors. For this reason, most previous approaches to this issue depend on individual-based simulations. However, simulation studies with only slightly different assumptions have come to wildly different conclusions, making it hard to generalize results and leading to fierce debate.

In a recent study published in The American Naturalist, Pleuni Pennings and her coworkers chose a different approach. They started out from a widely cited simulation model by Ulf Dieckmann and Michael Doebeli, who investigated sympatric speciation driven by resource competition. They then simplified the assumptions of this model to make it mathematically tractable. While retaining each of the crucial ingredients, Pennings et al. managed a completely analytical dissection of the model, something that had not appeared possible beforehand. They found that varying the model parameters produced phenomena that had previously been described in separate papers. "This means that our model unifies insights from earlier work, which is very rewarding," says Michael Kopp, one of the authors of the study. "We also gained a better understanding of the underlying mechanisms, such as the interplay of natural and sexual selection."

"Plants may alter competition by modifying nutrient bioavailability in rhizosphere: a modeling approach"
Xavier Raynaud (Université Paris-Sud and Université Pierre et Marie Curie-Paris), Benoît Jaillard (Laboratoire de Biogéochimie du Sol et de la Rhizosphère), and Paul W. Leadley (Université Paris-Sud)

Plants need nutrients such as Nitrogen and Phosphorus from the soil to grow. In temperate grasslands, several plant individuals can often be found on a small surface with their roots system thoroughly entwined. How plants share soil nutrients in these ecosystems has been the subject of debate between ecologists for decades, with several key questions still unanswered. In particular, few theories of plant competition account for the well-documented ability of plants to increase the availability of key soil nutrients by releasing protons or organic compounds from their roots. In order to study the consequences of the liberation of such compounds on competitive interactions between plants, Raynaud and his colleagues have developed a new model that simulates the release of these compounds and the uptake of nutrients by plants at the scale of individual roots. "Our model emphasizes the importance of soil water in determining the mobility of nutrients in the soil and therefore which plants will be able to get them," states Xavier Raynaud. "Roots behave essentially as independent units in dry soils, so plants interact primarily through the number of roots they make. However, in wet soils, plants can strongly influence their neighbors by releasing exudates from their roots or by rapidly taking up nutrients. We hope that this model will help unify divergent views of plant competition by providing a more comprehensive view of the mechanisms controlling nutrient fluxes in the soil."

"Nontrophic interactions, biodiversity, and ecosystem functioning: an interaction web model"
Alexandra Goudard (Ecole Normale Supérieure and Université Pierre et Marie Curie) and Michel Loreau (McGill University)

Most ecological theories deal with simple consumer-resource interactions. Scientists at Ecole Normale Supérieure (Paris) and McGill University provide a novel approach to incorporate nontrophic interactions, such as pollination and habitat modification, in ecosystem models, which allows them to study the dynamics of complex interaction webs.

Their model adds nontrophic interactions to a food web in the form of modifications of trophic interactions. It also tracks nutrient fluxes in the food web and hence satisfies the principle of mass conservation. Using this model, they show that nontrophic interactions can profoundly influence ecosystem properties such as species diversity, biomass, and production. In turn, the nature, prevalence, and strength of species interactions depend on species diversity. Counterintuitively, strong positive interactions tend to deteriorate ecosystem functioning because consumers become very efficient at exploiting their resources. "Nontrophic interactions are still poorly studied theoretically, and their impact on biodiversity and ecosystem functioning was largely unknown," says Michel Loreau, Canada Research Chair in theoretical ecology. "We hope that our new approach will boost their study and contribute to a more comprehensive theory of complex ecological systems. Organisms interact in many other ways than through feeding on each other or competing for shared resources," he adds. "Ecology should be able to account, not only for the diversity of species, but also for the diversity of their interactions."

"Mating frequency and inclusive fitness in Drosophila melanogaster"
Nicholas K. Priest (University of Virginia and Indiana University), Laura F. Galloway (University of Virginia), and Deborah A. Roach (University of Virginia)

Sexual conflict resolution?

In the gene's eye view, female mating frequency is difficult to understand. A substantial body of evidence, taken throughout the animal kingdom, demonstrates that females mate frequently, even when bouts of mating decrease offspring production. This finding is counterintuitive because we would expect natural selection to remove mating behaviors which decrease fitness. However, new research suggests that frequent mating females receive fitness benefits from an unexpected source: their daughters. Evolutionary Biologists from the University of Virginia - Nick Priest, Laura Galloway and Deborah Roach - manipulated the mating frequency of female fruit flies, Drosophila melanogaster, and observed how mating frequency affected the lifetime reproductive output of those females and their daughters. They found that frequent mating decreased maternal survival and reproductive output, but increased the reproductive output of daughters.

"Frequent mating was more hazardous to females than we had suspected," explains Priest, who conducted the study as part of his doctoral research. "Increased mating frequency actually accelerated the female aging process. But, the daughters of frequent mating mothers had enhanced offspring production." Are the benefits to daughters enough to recoup the costs of mating" The authors evaluated their data using a model of inclusive fitness which considered the multi-generation costs and benefits of frequent mating. They found that costs to mothers were balanced by benefits to daughters such that frequency mating was neither detrimental nor beneficial. This finding indicates that cross-generational fitness effects may play an important role in evolution of mating frequency in the fruit fly and may have a more general role in life history evolution.

That this phenomenon was discovered in the fruit fly is surprising. The fruit fly is often hailed as an example of sexual conflict, in part because males and females appeared to have conflicting optimal mating frequencies. But, the work of Priest and colleagues shows that the genes which determine mating frequency in females might actually spread faster, despite direct costs to females, when their effects are considered over multiple generations. "Sexual conflict might still have an important role in the evolution of mating behavior," states Priest. "But, clearly, we have to consider the fitness consequences of mating over more than one generation. Males and females are not in conflict with respect to mating frequency, as they both appear to benefit from frequent mating."

"Optimal cell size for resource uptake in fluids: a new facet of resource competition"
Kohei Yoshiyama and Christopher A. Klausmeier (Michigan State University)

Ecologists generally observe a positive relationship between sizes of predators and their prey, mainly because predators need to be large to eat a larger prey. But does this positive relationship hold for sizes of bacteria and their food molecules" Using a mathematical model, scientists at Michigan State University predict the opposite, an inverse relationship between sizes of bacteria and their resource molecules. Theoretical biologists Kohei Yoshyama and Chris Klausmeier tweaked a model of bacterial growth in an aqueous medium to account for resource transport from medium to the cell surface by molecular diffusion together with biological uptake processes, and derived a negative relationship between sizes of resource molecule and bacterial cell that is most efficient in the resource competition. They also showed that two bacterial consumers can coexist on two resources that are identical except for their sizes. This result implies that size differences of resource molecules, regardless of the quality, can promote microbial diversity. "Theoretically, smaller cells are more favored under transport limitation for resource uptake than under limitations by biological processes, such as membrane uptake or catalysis within cells. As resource molecules become smaller, the molecular diffusion speeds up. And then the transport limitation for resource uptake is relaxed, and the optimal cell size becomes larger," states Kohei Yoshiyama, the study's leading author. He adds, "Species diversity, at least at stable environments, is constrained by number of resources, which previously considered to be finite. Our results add a new dimension to the concept of 'resource', making the number of resources infinite."

University of Chicago Press Journals

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