The evolution of host-parasite range.

Understanding the coevolution of hosts and parasites is one of the key challenges for evolutionary biology. In particular, it is important to understand the processes that generate and maintain variation. Here, we examine a coevolutionary model of hosts and parasites where infection does not depend on absolute rates of transmission and defense but is approximately all-or-nothing, depending on the relative levels of defense and infectivity of the host and the parasite. We show that considerable diversity can be generated and maintained because of epidemiological feedbacks, with strains differing in the range of host and parasite types they can respectively infect or resist. Parasites with broad and narrow ranges therefore coexist, as do broadly and narrowly resistant hosts, but this diversity occurs without the assumption of highly specific gene interactions. In contrast to gene-for-gene models, cycling in strain types is found only under a restrictive set of circumstances. The generation of diversity in both hosts and parasites is dependent on the shape of the trade-off relationships but is more likely in long-lived hosts and chronic disease with long infectious periods. Overall, our model shows that significant diversity in infectivity and resistance range can evolve and be maintained from initially monomorphic populations.

Promiscuity and the primate immune system.

The behavioral and ecological factors involved in immune system evolution remain poorly explored. We present a phylogenetic analysis of white blood cell counts in primates to test three hypotheses related to disease risk: increases in risk are expected with group size or population density, exposure to soil-borne pathogens, and mating promiscuity. White blood cell counts were significantly greater in species where females have more mating partners, indicating that the risk of sexually transmitted disease is likely to be a major factor leading to systematic differences in the primate immune system.

Silene as a model system in ecology and evolution.

The genus Silene, studied by Darwin, Mendel and other early scientists, is re-emerging as a system for studying interrelated questions in ecology, evolution and developmental biology. These questions include sex chromosome evolution, epigenetic control of sex expression, genomic conflict and speciation. Its well-studied interactions with the pathogen Microbotryum has made Silene a model for the evolution and dynamics of disease in natural systems, and its interactions with herbivores have increased our understanding of multi-trophic ecological processes and the evolution of invasiveness. Molecular tools are now providing new approaches to many of these classical yet unresolved problems, and new progress is being made through combining phylogenetic, genomic and molecular evolutionary studies with ecological and phenotypic data.

Spatiotemporal dynamics in marginal populations.

Population dynamics across a mortality gradient at an ecological margin are investigated using a novel modeling approach that allows direct comparison of stochastic spatially explicit simulation results with deterministic mean field models. The results show that demographic stochasticity has a large effect at population margins such that density profiles fall off more sharply than predicted by mean field models. Substantial spatial structure emerges at the margin, and spatial correlations (measured parallel to the margin) exhibit a sharp maximum in the tail of the density profile, indicating that spatial substructuring is greatest at an intermediate point across the ecological gradient. Such substructuring may have a substantial impact on Allee effects and evolutionary processes in marginal populations.

The effects of environmental heterogeneity on the genetics of finite populations.

The effects on a panmictic population of a patchy environment and stochastic selection were investigated by computer simulation. The model allowed for different patterns and intensities of selection and various densities of distribution of the offspring. It delineated the effects of these variables on the correlation between the genotype and the environment, the level of heterozygosity, the change in gene frequency from generation to generation and the divergence between similar populations due to random effects.

Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success.

Studies of disease in relation to animal mating systems have focused on sexual selection and the evolution of sexual reproduction. Relatively little work has examined other aspects of ecological and evolutionary relationships between host social and sexual behaviour, and dynamics and prevalence of infectious diseases; this is particularly evident with respect to sexually transmitted diseases (STDs). Here, we use a simulation approach to investigate rates of STD spread in host mating systems ranging from permanent monogamy to serial polygyny or polyandry and complete promiscuity. The model assumes that one sex (female) is differentially attracted to the other, such that groups of varying size are formed within which mating and disease transmission occur. The results show that equilibrium disease levels are generally higher in females than males and are a function of variance in male mating success and the likelihood of a female switching groups between mating seasons. Moreover, initial rates of disease spread (determining whether an STD establishes in a population) depend on patterns of host movement between groups, variance in male mating success and host life history (e.g. mortality rates). Male reproductive success can be reduced substantially by a sterilizing STD and this reduction is greater in males that are more 'attractive' to females. In contrast, females that associate with more attractive males have lower absolute fitness than females associating with less attractive males. Thus, the potential for STDs to act as a constraint on directional selection processes leading to polygyny (or polyandry) is likely to depend on the details of mate choice and group dynamics.

Coexistence under positive frequency dependence.

Negative frequency dependence resulting from interspecific interactions is considered a driving force in allowing the coexistence of competitors. While interactions between species and genotypes can also result in positive frequency dependence, positive frequency dependence has usually been credited with hastening the extinction of rare types and is not thought to contribute to coexistence. In the present paper, we develop a stochastic cellular automata model that allows us to vary the scale of frequency dependence and the scale of dispersal. The results of this model indicate that positive frequency dependence will allow the coexistence of two species at a greater rate than would be expected from chance. This coexistence arises from the generation of banding patterns that will be stable over long time-periods. As a result, we found that positive frequency-dependent interactions over local spatial scales promote coexistence over neutral interactions. This result was robust to variation in boundary conditions within the simulation and to variation in levels of disturbance. Under all conditions, coexistence is enhanced as the strength of positive frequency-dependent interactions is increased.

The measurement of small-scale environmental heterogeneity using clonal transplants of Anthoxanthum odoratum and Danthonia spicata.

To assess the scale of micro-environmental heterogeneity perceived by two co-occurring grass species, Anthoxanthum odoratum and Danthonia spicata, cloned tillers of each species were planted into the natural habitat at a range of spacings (from 2 cm to more than 2 m apart) and measured for survival and fecundity over three years. A. odoratum responded to heterogeneity at a scale of 4-8 cm and at a scale of 2-8 m but not to intermediate scales. D. spicata did not respond significantly to heterogeneity. However one genotype infected with the systemic fungus Atkinsonella hypoxylon showed a large response to heterogeneity at both small and large spatial scales. The results showed that the scale and level of environmental heterogeneity as measured by its fitness impact depends on the species and genotype involved. The results indicate that small scale environmental heterogeneity could play a role in the maintenance of sexual reproduction in A. odoratum.

Is atmospheric CO2 a selective agent on model C3 annuals?

Atmospheric CO2 partial pressure (pCO2) was as low as 18 Pa during the Pleistocene and is projected to increase from 36 to 70 Pa CO2 before the end of the 21st century. High pCO2 often increases the growth and reproduction of C3 annuals, whereas low pCO2 decreases growth and may reduce or prevent reproduction. Previous predictions regarding the effects of high and low pCO2 on C3 plants have rarely considered the effects of evolution. Knowledge of the potential for evolution of C3 plants in response to CO2 is important for predicting the degree to which plants may sequester atmospheric CO2 in the future, and for understanding how plants may have functioned in response to low pCO2 during the Pleistocene. Therefore, three studies using Arabidopsis thaliana as a model system for C3 annuals were conducted: (1) a selection experiment to measure responses to selection for high seed number (a major component of fitness) at Pleistocene (20 Pa) and future (70 Pa) pCO2 and to determine changes in development rate and biomass production during selection, (2) a growth experiment to determine if the effects of selection on final biomass were evident prior to reproduction, and (3) a reciprocal transplant experiment to test if pCO2 was a selective agent on Arabidopsis. Arabidopsis showed significant positive responses to selection for high seed number at both 20 and 70 Pa CO2 during the selection process. Furthermore, plants selected at 20 Pa CO2 performed better than plants selected at 70 Pa CO2 under low CO2 conditions, indicating that low CO2 acted as a selective agent on these annuals. However, plants selected at 70 Pa CO2 did not have significantly higher seed production than plants selected at 20 Pa CO2 when grown at high pCO2. Nevertheless, there was some evidence that high CO2 may also be a selective agent because changes in development rate and biomass production during selection occurred in opposite directions at low and high pCO2. Plants selected at high pCO2 showed no change or reductions in biomass relative to control plants due to a decrease in the length of the life cycle, as indicated by earlier initiation of flowering and senescence. In contrast, selection at low CO2 resulted in an average 35% increase in biomass production, due to an increase in the length of the life cycle that resulted in a longer period for biomass accumulation before senescence. From the Arabidopsis model system we conclude that some C3 annuals may have produced greater biomass in response to low pCO2 during the Pleistocene relative to what has been predicted from studies exposing a single generation of C3 plants to low pCO2. Furthermore, C3 annuals may exhibit evolutionary responses to high pCO2 in the future that may result in developmental changes, but these are unlikely to increase biomass production. This series of studies shows that CO2 may potentially act as a selective agent on C3 annuals, producing changes in development rate and carbon accumulation that could not have been predicted from single-generation studies.

Emerging and reemerging infectious diseases: a multidisciplinary perspective.

Predictions that infectious diseases would be eliminated as a major threat to human health have been shattered by emerging and reemerging infections, among them acquired immunodeficiency syndrome (AIDS), hemorrhagic fevers, marked increases in infections caused by antimicrobial-resistant bacteria, and the resurgence of tuberculosis and malaria. Understanding the dynamics of emerging and reemerging infections is critical to efforts to reduce the morbidity and mortality of such infections, to establish policy related to preparedness for infectious threats, and for decisions on where to use limited resources in the fight against infections. In order to offer a multidisciplinary perspective, 23 infectious disease specialists, epidemiologists, geneticists, microbiologists, and population biologists participated in an open forum at Emory University on emerging and reemerging infectious diseases. As summarized below, the group addressed questions about the definition, the identification, the factors responsible for, and multidisciplinary approaches to emerging and reemerging infections.

Evolution in closely adjacent plant populations X: long-term persistence of prereproductive isolation at a mine boundary.

Flowering time differences between metal-tolerant and nontolerant populations of the grass Anthoxanthum odoratum growing across a mine boundary have persisted for over 40 years. These flowering time differences result in a high degree of prezygotic genetic isolation (isolation index=0.43) between the tolerant mine populations and nontolerant pasture populations. Previous work showing genetic determination of flowering time and a high turnover of individual plants argues strongly for the selective maintenance of this difference.

Wilhelm Ludwig and his contributions to population genetics.

This article reviews the life and work of the German biologist Wilhelm Ludwig (1901-1959), whose contributions to population genetics have been largely ignored. Ludwig's work was a rich tapestry of population biology, spanning investigations into population growth, biological asymmetries, sex ratio, and paternity analysis. He was ahead of his time in explicitly combining the theory of population ecology and population genetics. His classic paper on annidation showed the possibility of population differentiation in the face of gene flow, and his early studies demonstrated the importance of selection in evolutionary change. Much of his work spanned the period of the Second World War in Germany, and interesting questions remain about his life during this turbulent period.

Frequency-dependent selection and competition: empirical approaches.

When Darwin and Wallace first formulated the theory of evolution by natural selection, they were greatly influenced by the idea that populations tend to increase geometrically and rapidly outgrow the resources available to them. They argued that the ensuing competition among individuals would be a major agent of natural selection. Since their day, competition has become almost synonymous with the idea of natural selection or survival of the fittest. In this paper we examine the relation between competition and selection by using simple competition models, consider the interaction of density and frequency in determining competitive outcome, and review the literature on frequency-dependent competitive interactions among genotypes within populations.

Intratetrad mating, heterozygosity, and the maintenance of deleterious alleles in Microbotryum violaceum (=Ustilago violacea).

The mating system of Microbotryum violaceum was investigated in populations that are polymorphic for mating-type bias, where individuals produce viable haploids of only one of the two required mating types. The cause of mating-type bias was identified as deleterious recessive alleles linked to mating type. Maintenance of the deleterious alleles was promoted by early conjugation among products of single meioses, such that the duration of the free-living haploid stage is minimized. This development was also observed in nonbiased isolates. As a consequence, the mating system tends toward mating within the tetrad, which might be expected to reduce heterozygosity. However, complete centromere linkage of mating type ensures conjugation between first division meiotic products, such that mating in M. violaceum is analogous to forms of meiotic parthenogenesis with first division restitution (i.e. automixis with central fusion). This fungus was used to test the prediction that this mating system would maintain heterozygosity in regions of the genome linked to centromeres. Therefore, populations were screened for additional heterozygous lethal recessive alleles linked to centromeres, and several examples were found. Furthermore, the occurrence of intratetrad mating in M. violaceum provides an explanation for low variation among individuals within populations, inconsistent estimates of outcrossing rates, low levels of mating between tetrads of one diploid individual, and high frequencies of haplo-lethal alleles in natural populations.

Ontoecogenophyloconstraints? The chaos of constraint terminology.

The world of evolutionary biology today is being bombarded with all kinds of possible constraints to the process of natural selection. Are we witnessing the end of the neodarwinistic theory of evolution, as some may like to see it, or is it just another whim of giving new names to old things? Here, we attempt to unravel the meaning and name-giving of constraints in a small and nonrandom sample of the literature, and suggest a way out from the present confusion of usages.

Correlation between male and female reproduction in the subdioecious herb Astilbe biternata (Saxifragaceae).

Genotypic trade-offs between male and female reproduction are commonly assumed in theoretical studies of the evolution of gender specialization. Although these trade-offs are supported by higher seed production of females than hermaphrodites in natural populations of gynodioecious species, comparisons between male and female reproductive allocation among hermaphrodite individuals under controlled conditions are rare. We assessed phenotypic and genotypic correlations between stamen and fruit production in fruiting males of the near-dioecious herb Astilbe biternata. In the field, we found a significant negative phenotypic correlation between stamen production and fruit production within individuals that produced both stamens and fruit as well as higher fruit set in females than fruiting males. The negative correlation between fruit and stamen production that was observed in the field was also apparent across clonally propagated genotypes. These results suggest that negative genetic correlations between male and female reproduction may limit the independent evolution of fruit and stamen production in A. biternata.

Sexually transmitted diseases in animals: ecological and evolutionary implications.

Sexually transmitted diseases (STDs) have been generally thought of as a small subset of infectious diseases, rather than as an important group of diseases that occur in numerous species. In this paper, we have (1) briefly reviewed theoretical studies on the dynamics of STDs; (2) documented the distribution of STDs in the animal kingdom; and (3) investigated whether STDs have characteristics which distinguish them from other infectious diseases. The dynamics of STDs should differ from those of ordinary infectious diseases because their transmission depends on the frequency rather than density of infectives. With this type of transmission, there is no threshold density for disease spread, and the conditions for host-pathogen coexistence are more restrictive. Nevertheless, a wide variety of disease characteristics may allow a sexually transmitted pathogen to coexist with its host. We found over 200 diseases for which there was evidence of sexual transmission. They occurred in groups as diverse as mammals, reptiles, arachnids, insects, molluscs and nematodes. Sexually transmitted pathogens included protozoans, fungi, nematodes, helminths, and cancerous cell lines, as well as bacteria and viruses. Detailed comparison of the characteristics of sexually transmitted mammalian diseases with those that are transmitted by non-sexual means, showed that STDs cause less mortality, are longer-lived in their hosts, are less likely to invoke strong immune responses, have narrower host-ranges, and show less fluctuation in prevalence over time. These shared features are related to mode of transmission rather than either host or pathogen taxonomic affiliation. This suggests an evolutionary explanation based on shared ecologies rather than one based on phylogenetic history.

Population dynamics with global regulation: the conserved Fisher equation.

We introduce and study a conserved version of the Fisher equation. Within a population biology context, this model describes spatially extended populations in which the total number of individuals is fixed due to either biotic or environmental factors. We find a rich spectrum of dynamical phases including a pseudotraveling wave and, in the presence of the Allee effect, a phase transition from a locally constrained high density state to a low density fragmented state.

Allocation to sexual versus nonsexual disease transmission.

Many diseases have both sexual and nonsexual transmission routes, and closely related diseases often differ in their degree of sexual transmission. We investigate the evolution of transmission mode as a function of host social and mating structure using a model in which disease transmission is explicitly dependent on the numbers of sexual and nonsexual contacts (which are themselves a function of population density) and per-contact infection probabilities. Most generally, and in the absence of trade-offs between the degree of sexual transmission and effects on host fecundity and mortality, nonsexual transmission is favored above the social-sexual crossover point (the host density at which the number of nonsexual contacts exceeds the number of sexual contacts), while sexual transmission is favored below this point. When changes in allocation to the two transmission modes are accompanied by changes in mortality or fecundity, both mixed and pure transmission strategies can be favored. If invading genotypes differ substantially from resident genotypes, genetic polymorphism in transmission mode is possible. The evolutionary outcomes are predictable from a knowledge of the equilibrium population sizes in relation to the social-sexual crossover point. Our results also show that predictions about dynamic outcomes, based on rates of invasion for single pathogens into healthy populations, do not adequately describe the resulting disease prevalence nor predict the subsequent evolutionary dynamics; once invasion of a pathogen has occurred, the conditions for spread of a second pathogen are themselves altered. If the host is considered as a single resource, our results show that two pathogens may coexist on a single resource if they use that resource differentially and have differential feedbacks on resource abundance; such resource feedback effects may be present in other biological systems.