The ecological advantage of sexual reproduction in multicellular long-lived organisms

We present a model for the advantage of sexual reproduction in multicellular long-lived species in a world of structured resources in short supply. The model combines features of the Tangled Bank and the Red Queen hypothesis of sexual reproduction and is of broad applicability. The model is ecologically explicit with the dynamics of resources and consumers being modelled by differential equations. The life history of consumers is shaped by body mass-dependent rates as implemented in the metabolic theory of ecology. We find that over a broad range of parameters, sexual reproduction wins despite the two-fold cost of producing males, due to the advantage of producing offspring that can exploit underutilized resources. The advantage is largest when maturation and production of offspring set in before the resources of the parents become depleted, but not too early, due to the cost of producing males. The model thus leads to the dominance of sexual reproduction in multicellular animals living in complex environments, with resource availability being the most important factor affecting survival and reproduction.     

Mutation surfing and the evolution of dispersal during range expansions

A growing body of empirical evidence demonstrates that at an expanding front, there can be strong selection for greater dispersal propensity, whereas recent theory indicates that mutations occurring towards the front of a spatially expanding population can sometimes ‘surf’ to high frequency and spatial extent. Here, we consider the potential interplay between these two processes: what role may mutation surfing play in determining the course of dispersal evolution and how might dispersal evolution itself influence mutation surfing? Using an individual‐based coupled‐map lattice model, we first run simulations to determine the fate of dispersal mutants that occur at an expanding front. Our results highlight that mutants that have a slightly higher dispersal propensity than the wild type always have a higher survival probability than those mutants with a dispersal propensity lower than, or very similar to, the wild type. However, it is not always the case that mutants with very high dispersal propensity have the greatest survival probability. When dispersal mortality is high, mutants of intermediate dispersal survive most often. Interestingly, the rate of dispersal that ultimately evolves at an expanding front is often substantially higher than that which confers a novel mutant with the greatest probability of survival. Second, we run a model in which we allow dispersal to evolve over the course of a range expansion and ask how the fate of a neutral or nonneutral mutant depends upon when and where during the expansion it arises. These simulations highlight that the success of a neutral mutant depends upon the dispersal genotypes that it is associated with. An important consequence of this is that novel mutants that arise at the front of an expansion, and survive, typically end up being associated with more dispersive genotypes than the wild type. These results offer some new insights into causes and the consequences of dispersal evolution during range expansions, and the methodology we have employed can be readily extended to explore the evolutionary dynamics of other life history characteristics.     

Maternal effects and heritability of annual productivity

Within-individual consistency and among-individual heterogeneity in fitness are prerequisites for selection to take place. Within-individual variation in productivity between years, however, can vary considerably, especially when organisms become older and more experienced. We examine individual consistency in annual productivity, the covariation between survival and annual productivity, and the sources of variation in annual productivity, while accounting for advancing age, to test the individual-quality and resource-allocation life-history theory hypotheses. We use long-term data from a pedigreed, wild population of house sparrows. Within-individual annual productivity first increased and later decreased with age, but there were no selective mortality due to individual quality and no correlation between lifespan and productivity. Individuals were consistent in their annual productivity (C = 0.49). Narrow-sense heritability was low (h(2) = 0.09), but maternal effects explained much of the variation (M = 0.33). Such effects can influence evolutionary processes and are of major importance for our understanding of how variation in fitness can be maintained.     

Estimating dispersal rate of the silky cane weevil (Coleoptera: Curculionidae)*

Abstract: The objective of this study was to estimate the silky cane weevil rate of dispersal under near‐natural conditions inside a screened enclosure where an array of buckets was baited with cut sugarcane stalks. One hundred weevils were released and weevils inside the buckets were counted hourly for 8 h, and then 24 and 48 h after release. A passive diffusion model was used to estimate the weevil's dispersal and disappearance rates, within and between rows of buckets with sugarcane. The weevils concentrated around the release point and slowly moved towards the boundaries of the experimental plot over time with an overall average dispersal rate of 2.8 ± 3.58 cm²/h. Dispersal and disappearance rates within and between rows were not significantly different among the time intervals considered (1–8, 8–24 and 24–48 h after release) except for the 1–8 time interval on the array representing the release point when the dispersal rate, D, was significantly higher than those at other time intervals. Continuum of the substratum to disperse from one side of the array to another via a wooden bridge may explain the higher dispersal rate through this array. The number of buckets exposed to the sun during the morning hours was significantly higher on those rows exposed to the sun (south side of the screen enclosure) than on the shaded side. Longer times of bucket exposure to the sun may explain the predominant distribution of weevils in that area suggesting that the weevil population is constantly expanding and retracting according to micro environmental conditions.     

The evolution of dispersal polymorphisms in insects: The influence of habitats,host plants and mates

Wing-dimorphic, delphacid planthoppers were used to test hypotheses concerning the effects of habitat persistence and architectural complexity on the occurrence of dispersal. For reasons concerning both the durational stability of the habitat and the reduced availability of mates, selection has favored high levels of dispersal in species occupying temporary habitats. Flightlessness predominates in species occupying persistent habitats, and is promoted by a phenotypic trade-off between reproductive success and flight capability. Wings are retained in tree-inhabiting species, probably for reasons concerning the more effective negotiation of three-dimensional habitats. In contrast, flightlessness is characteristic of those species inhabiting low profile host plants. For several delphacid genera, migratory species are larger than their sedentary congeners. Because body size and fecundity are positively related in planthoppers, the large body size observed in migratory taxa may result from selection for increased fecundity in colonizing species.     

Introduction. Evolutionary dynamics of wild populations: the use of long-term pedigree data

Studies of populations in the wild can provide unique insights into the forces driving evolutionary dynamics. This themed issue of Proc. R. Soc. B focuses on new developments in long-term analyses of animal populations where pedigree information has been collected. These address fundamental questions in evolutionary biology concerning the genetic basis of phenotypic diversity, patterns of natural and sexual selection, the occurrence of inbreeding and inbreeding depression, and speciation. Contributions include the analysis of evolutionary responses to climate change, exploration of the genetic basis of senescence, the exploitation of advances in molecular genetic technology, and reviews of developments in quantitative genetic methodology. We discuss here common themes, specific problems and pointers for future research.     

Haemosporidian vector research: marriage of molecular and microscopical approaches is essential

Many species of malaria and related haemosporidian parasites (Haemosporida) are responsible for diseases in wild and domestic animals. These pathogens are exclusively transmitted by blood-sucking dipteran insects (Diptera). Traditional vector studies, which are based mainly on experimental infection and subsequent dissection of insects, are time-consuming, so progress in the identification of the vectors has been slow. Since the discovery of haemosporidians in wildlife by V. Danilewsky in 1884, it took over 70 years to determine the main vector groups of these parasites. However, precise vector-parasite relationships remain insufficiently investigated in wildlife, particularly at the species level of haemosporidians and their vectors. Molecular tools have provided innovative opportunities to speed such research. In this issue of Molecular Ecology, Martínez-de la Puente et al. (2011) collected, for the first time, a significant PCR-based set of data on the presence of lineages of the pigment-forming haemosporidians (species of Haemoproteus and Plasmodium) in biting midges (Culicoides). They identified numerous associations between Culicoides spp. and Haemoproteus spp., indicating directions for future targeting vector studies of haemoproteids.     

The trade‐off between rate and yield in the design of microbial metabolism

Extra energy devoted to resource acquisition speeds metabolic rate, but reduces the net yield of energy. In direct competition, microbial strains with high rates of resource acquisition often outcompete strains with slower resource acquisition but higher yield, reducing the net output of the group. Here, I use mathematical models to analyse the genetic and demographic factors that tip the balance toward either rate or yield. My models clarify the widely discussed roles of kin selection and the spatial structure of populations. I also emphasize the strong effect of two previously ignored factors: demographic aspects of colony survival and reproduction strongly shape the design of metabolic rate and efficiency, and competitive mutants within long‐lived colonies favour rate over yield, degrading the efficiency of the population.     

Testing hypotheses on the dispersal and evolutionary history of freshwater mussels (Mollusca: Bivalvia: Unionidae)

The relationship between dispersal and differentiation of the European freshwater mussel Unio pictorum (Linnaeus, 1758) was studied with molecular genetic methods. Forty‐two populations from France, Italy and central Europe were analysed. Genetic relationships were assessed from the geographical distribution of allele frequencies at 17 enzyme loci. Neighbouring groups of populations show small to moderate mean genetic distances (0.020 < D_mean < 0.263). With a few exceptions the genetic affinities of the populations are the closest within the same drainage basin. In central Europe and Northern Italy genetic differences between drainage systems are relatively large. Populations from north‐eastern Italy are genetically similar to Danubian populations. Mussels from the islands of Corsica and Sardinia are more closely related to populations from the Italian peninsula than to French populations from the Rhône drainage system. Genetic relationships within U. pictorum from central Europe reflect palaeogeographical relationships between river systems during the Pliocene and Pleistocene. Literature data on two North American unionid species and one European fish species show the same relationship between genetic diversity and the history of drainage systems, although the correlations are less strong. In France and Italy this correspondence is much less evident. Population dynamic processes and human activities leading to populational bottlenecks might have obscured it.     

Generation time,life history and the substitution rate of neutral mutations

Our understanding of molecular evolution is hampered by a lack of quantitative predictions about how life-history (LH) traits should correlate with substitution rates. Comparative studies have shown that neutral substitution rates vary substantially between species, and evidence shows that much of this diversity is associated with variation in LH traits. However, while these studies often agree, some unexplained and contradictory results have emerged. Explaining these results is difficult without a clear theoretical understanding of the problem. In this study, we derive predictions for the relationships between LH traits and substitution rates in iteroparous species by using demographic theory to relate commonly measured life-history traits to genetic generation time, and by implication to neutral substitution rates. This provides some surprisingly simple explanations for otherwise confusing patterns, such as the association between fecundity and substitution rates. The same framework can be applied to more complex life histories if full life-tables are available.     

REVIEW: Optimality models in the age of experimental evolution and genomics

Optimality models have been used to predict evolution of many properties of organisms. They typically neglect genetic details, whether by necessity or design. This omission is a common source of criticism, and although this limitation of optimality is widely acknowledged, it has mostly been defended rather than evaluated for its impact. Experimental adaptation of model organisms provides a new arena for testing optimality models and for simultaneously integrating genetics. First, an experimental context with a well‐researched organism allows dissection of the evolutionary process to identify causes of model failure – whether the model is wrong about genetics or selection. Second, optimality models provide a meaningful context for the process and mechanics of evolution, and thus may be used to elicit realistic genetic bases of adaptation – an especially useful augmentation to well‐researched genetic systems. A few studies of microbes have begun to pioneer this new direction. Incompatibility between the assumed and actual genetics has been demonstrated to be the cause of model failure in some cases. More interestingly, evolution at the phenotypic level has sometimes matched prediction even though the adaptive mutations defy mechanisms established by decades of classic genetic studies. Integration of experimental evolutionary tests with genetics heralds a new wave for optimality models and their extensions that does not merely emphasize the forces driving evolution.     

Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implications for the evolution of sex

Asexual reproduction could offer up to a two‐fold fitness advantage over sexual reproduction, yet higher organisms usually reproduce sexually. Even in facultatively parthenogenetic species, where both sexual and asexual reproduction is sometimes possible, asexual reproduction is rare. Thus, the debate over the evolution of sex has focused on ecological and mutation‐elimination advantages of sex. An alternative explanation for the predominance of sex is that it is difficult for an organism to accomplish asexual reproduction once sexual reproduction has evolved. Difficulty in returning to asexuality could reflect developmental or genetic constraints. Here, we investigate the role of genetic factors in limiting asexual reproduction in Nauphoeta cinerea, an African cockroach with facultative parthenogenesis that nearly always reproduces sexually. We show that when N. cinerea females do reproduce asexually, offspring are genetically identical to their mothers. However, asexual reproduction is limited to a nonrandom subset of the genotypes in the population. Only females that have a high level of heterozygosity are capable of parthenogenetic reproduction and there is a strong familial influence on the ability to reproduce parthenogenetically. Although the mechanism by which genetic variation facilitates asexual reproduction is unknown, we suggest that heterosis may facilitate the switch from producing haploid meiotic eggs to diploid, essentially mitotic, eggs.     

Age-dependency in hunting ability among the Ache of eastern Paraguay

This paper examines changes in hunting ability across the lifespan for the Ache of eastern Paraguay. Hunting ability is decomposed into two components-finding prey and probability of kill upon encounter- and analyzed for important prey species. Results support the argument that skill acquisition is an important aspect of the human foraging niche with hunting outcome variables reaching peaks surprisingly late in life, significantly after peaks in strength. The implications of this study are important for modeling the role of the human foraging niche in the co-evolution of various outstanding human life history characteristics such as large brains, long lifespans, and extended juvenile periods.     

Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern,rate, and process

Chinook salmon, Oncorhynchus tshawytscha, from the Sacramento River, California, USA were introduced to New Zealand between 1901 and 1907, and colonized most of their present-day range within about 10 years. The New Zealand populations now vary in phenotypic traits typically used to differentiate salmon populations within their natural range: growth in freshwater and at sea, age at maturity, dates of return to fresh water and reproduction, morphology, and reproductive allocation. This paper reviews a large research program designed to determine the relative contributions of phenotypic plasticity and genetic adaptation to this variation, in an effort to understand the processes underlying the natural evolution of new populations. We found strong evidence of trait divergence between populations within at most 30 generations, particularly in freshwater growth rate, date of return, and reproductive output, with plausible adaptive bases for these differences. Importantly, we also demonstrated not only a genetic basis for post-release survival but higher survival, and hence fitness, of a population released from its established site compared to another population released from the same site. We conclude that divergence of salmon in different rivers probably resulted initially from phenotypic plasticity (e.g., habitat-specific growth rates, and effects of upriver migration on ovarian investment). Philopatry (homing to natal streams) combined with rapid evolution of distinct breeding periods to restrict gene flow, facilitating divergence in other traits. We also suggest that in addition to genetic divergence resulting from random founder effects, divergence may also arise during the very early stages of colonization when the original colonists are a non-random, pre-adapted subset of the source population. This favored founders effect immediately improves the fitness of the new population. Overall, this research reveals the complex interplay of environmental and genetic controls over behavior, physiology and life history that characterize the early stages of population differentiation, a process that has taken place repeatedly during the history of salmon populations.     

Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions

Invasive species are predicted to suffer from reductions in genetic diversity during founding events, reducing adaptive potential. Integrating evidence from two literature reviews and two case studies, we address the following questions: How much genetic diversity is lost in invasions? Do multiple introductions ameliorate this loss? Is there evidence for loss of diversity in quantitative traits? Do invaders that have experienced strong bottlenecks show adaptive evolution? How do multiple introductions influence adaptation on a landscape scale? We reviewed studies of 80 species of animals, plants, and fungi that quantified nuclear molecular diversity within introduced and source populations. Overall, there were significant losses of both allelic richness and heterozygosity in introduced populations, and large gains in diversity were rare. Evidence for multiple introductions was associated with increased diversity, and allelic variation appeared to increase over long timescales (~100 years), suggesting a role for gene flow in augmenting diversity over the long‐term. We then reviewed the literature on quantitative trait diversity and found that broad‐sense variation rarely declines in introductions, but direct comparisons of additive variance were lacking. Our studies of Hypericum canariense invasions illustrate how populations with diminished diversity may still evolve rapidly. Given the prevalence of genetic bottlenecks in successful invading populations and the potential for adaptive evolution in quantitative traits, we suggest that the disadvantages associated with founding events may have been overstated. However, our work on the successful invader Verbascum thapsus illustrates how multiple introductions may take time to commingle, instead persisting as a ‘mosaic of maladaptation’ where traits are not distributed in a pattern consistent with adaptation. We conclude that management limiting gene flow among introduced populations may reduce adaptive potential but is unlikely to prevent expansion or the evolution of novel invasive behaviour.     

The adaptive legacy of human evolution: A search for the environment of evolutionary adaptedness

The growth of evolutionary psychology has led to renewed interest in what might be the significant evolutionary heritage of people living today, and in the extent to which humans are suited to a particular adaptive environment—the EEA. The EEA, though, is a new tool in the battery of evolutionary concepts, and it is important both that it is scrutinized for its utility, and that the actual reconstructions of the environments in which humans and hominids evolved are based on sound palaeobiological inference and an appropriate use of the phylogenetic context of primate evolution.     

New insight into the phylogenetic and biogeographic history of genus Ficus: Vicariance played a relatively minor role compared with ecological opportunity and dispersal

Studies on the evolution of tropical taxa emphasize the role ofvicariance and the break-up of Gondwana in explaining modern distributions.Earlier studies on figs (Ficus spp.) support this view.In the current study,we used an expanded sample (208 spp.) and improved molecular dating techniques to reconstruct the phylogenetic and biogeographic history of Ficus.Consistent with previous studies,our biogeographic analysis indicated that the ancestor of Ficus was present in Gondwana.However,a relaxed clock analysis relying on uncorrelated rates in BEAST suggested that the Neotropical section Pharmacosycea split-off in South America 86.67 Mya,and that other Ficus lineage ancestors originated in India.Most of the basal lineages appeared to have diverged following KT extinction,then rapidly diversified after India collided with continental Asia.The Afrotropical species most likely evolved initially in the Indian subcontinent then dispersed to Africa,either in the late Cretaceous of Madagascar or even later,following the Eocene collision of India with Asia.The Neotropical section Americana,either islandhopped to South America or took a northern route to the Americas through Europe prior to the terminal Eocene global cooling event.Ficus may have arrived in eastern Malesia following the collision of India with Asia,then widely dispersed thereafter.Given the wide ranges in our date estimates,several other scenarios are possible.However,contrary to earlier reports,our analyses suggest that vicariance played a relatively minor role compared with ecological opportunity and dispersal in the diversification of genus Ficus.