Evolution of adaptive phenotypic traits without positive Darwinian selection

Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.     

Introduction. Antarctic ecology: from genes to ecosystems. Part 2. Evolution, diversity and functional ecology

The Antarctic biota has evolved over the last 100 million years in increasingly isolated and cold conditions. As a result, Antarctic species, from micro-organisms to vertebrates, have adapted to life at extremely low temperatures, including changes in the genome, physiology and ecological traits such as life history. Coupled with cycles of glaciation that have promoted speciation in the Antarctic, this has led to a unique biota in terms of biogeography, patterns of species distribution and endemism. Specialization in the Antarctic biota has led to trade-offs in many ecologically important functions and Antarctic species may have a limited capacity to adapt to present climate change. These include the direct effects of changes in environmental parameters and indirect effects of increased competition and predation resulting from altered life histories of Antarctic species and the impacts of invasive species. Ultimately, climate change may alter the responses of Antarctic ecosystems to harvesting from humans. The unique adaptations of Antarctic species mean that they provide unique models of molecular evolution in natural populations. The simplicity of Antarctic communities, especially from terrestrial systems, makes them ideal to investigate the ecological implications of climate change, which are difficult to identify in more complex systems.     

Predictive ecology: systems approaches

The world is experiencing significant, largely anthropogenically induced, environmental change. This will impact on the biological world and we need to be able to forecast its effects. In order to produce such forecasts, ecology needs to become more predictive--to develop the ability to understand how ecological systems will behave in future, changed, conditions. Further development of process-based models is required to allow such predictions to be made. Critical to the development of such models will be achieving a balance between the brute-force approach that naively attempts to include everything, and over simplification that throws out important heterogeneities at various levels. Central to this will be the recognition that individuals are the elementary particles of all ecological systems. As such it will be necessary to understand the effect of evolution on ecological systems, particularly when exposed to environmental change. However, insights from evolutionary biology will help the development of models even when data may be sparse. Process-based models are more common, and are used for forecasting, in other disciplines, e.g. climatology and molecular systems biology. Tools and techniques developed in these endeavours can be appropriated into ecological modelling, but it will also be necessary to develop the science of ecoinformatics along with approaches specific to ecological problems. The impetus for this effort should come from the demand coming from society to understand the effects of environmental change on the world and what might be performed to mitigate or adapt to them.     

Toward a synthetic understanding of the role of phenology in ecology and evolution

Phenology affects nearly all aspects of ecology and evolution. Virtually all biological phenomena—from individual physiology to interspecific relationships to global nutrient fluxes—have annual cycles and are influenced by the timing of abiotic events. Recent years have seen a surge of interest in this topic, as an increasing number of studies document phenological responses to climate change. Much recent research has addressed the genetic controls on phenology, modelling techniques and ecosystem-level and evolutionary consequences of phenological change. To date, however, these efforts have tended to proceed independently. Here, we bring together some of these disparate lines of inquiry to clarify vocabulary, facilitate comparisons among habitat types and promote the integration of ideas and methodologies across different disciplines and scales. We discuss the relationship between phenology and life history, the distinction between organismal- and population-level perspectives on phenology and the influence of phenology on evolutionary processes, communities and ecosystems. Future work should focus on linking ecological and physiological aspects of phenology, understanding the demographic effects of phenological change and explicitly accounting for seasonality and phenology in forecasts of ecological and evolutionary responses to climate change.     

Seedling-selection effects on morphological traits of mature plants in red clover

Knowledge of the correlation between juvenileand mature-plant traits is critical in determining the opportunities for early stage selection. The effects of early stage selection on mature-plant performance have rarely been quantified. This study was conducted to identify seedling traints in red clover (Trifolium pratense L.) that correlate to mature-plant traits and to evaluate the effect of seedling selection on forage yields and other mature-plant traits. The results showed that relationships between most seedlingand mature-plant traits were weak (r ranged from 0.170 to 0.239). Nevertheless, selecting the top 10% seedlings for petiole length, days from emergence to full expansion of the 4th leaf (D4LE), or leaves per seedling, produced a mature-plant population with higher individual plant dry weight (IPDW1) and higher annual yield in 1993 (Y93). Selection for leaves per seedling increased IPDW1 by 23.2%. Selection for petiole length and the smallest D4LE increased Y93 by 15.7% and 13.8%, respectively. Furthermore, substantial expected genetic gains were obtained for IPDW1 and Y93 when selecting for some seedling traits. We conclude that plants and families with low potential yield can be eliminated at the seedling stage in red clover. This will allow breeders to increase the number of superior plants to be field tested or to conduct a more rigorous evaluation of the selected plants. Among the five selection schemes tested for direct selection of mature-plant traits, mass selection produced the largest genetic gain.     

Climate change and the risks associated with delayed breeding in a tropical wild bird population

There is growing evidence of changes in the timing of important ecological events, such as flowering in plants and reproduction in animals, in response to climate change, with implications for population decline and biodiversity loss. Recent work has shown that the timing of breeding in wild birds is changing in response to climate change partly because individuals are remarkably flexible in their timing of breeding. Despite this work, our understanding of these processes in wild populations remains very limited and biased towards species from temperate regions. Here, we report the response to changing climate in a tropical wild bird population using a long-term dataset on a formerly critically endangered island endemic, the Mauritius kestrel. We show that the frequency of spring rainfall affects the timing of breeding, with birds breeding later in wetter springs. Delays in breeding have consequences in terms of reduced reproductive success as birds get exposed to risks associated with adverse climatic conditions later on in the breeding season, which reduce nesting success. These results, combined with the fact that frequency of spring rainfall has increased by about 60 per cent in our study area since 1962, imply that climate change is exposing birds to the stochastic risks of late reproduction by causing them to start breeding relatively late in the season.     

Pollination ecology and the possible impacts of environmental change in the Southwest Australian Biodiversity Hotspot

The Southwest Australian Biodiversity Hotspot contains an exceptionally diverse flora on an ancient, low-relief but edaphically diverse landscape. Since European colonization, the primary threat to the flora has been habitat clearance, though climate change is an impending threat. Here, we review (i) the ecology of nectarivores and biotic pollination systems in the region, (ii) the evidence that trends in pollination strategies are a consequence of characteristics of the landscape, and (iii) based on these discussions, provide predictions to be tested on the impacts of environmental change on pollination systems. The flora of southwestern Australia has an exceptionally high level of vertebrate pollination, providing the advantage of highly mobile, generalist pollinators. Nectarivorous invertebrates are primarily generalist foragers, though an increasing number of colletid bees are being recognized as being specialized at the level of plant family or more rarely genus. While generalist pollination strategies dominate among insect-pollinated plants, there are some cases of extreme specialization, most notably the multiple evolutions of sexual deception in the Orchidaceae. Preliminary data suggest that bird pollination confers an advantage of greater pollen movement and may represent a mechanism for minimizing inbreeding in naturally fragmented populations. The effects of future environmental change are predicted to result from a combination of the resilience of pollination guilds and changes in their foraging and dispersal behaviour.     

Prediction of genetic values of quantitative traits with epistatic effects in plant breeding populations

Though epistasis has long been postulated to have a critical role in genetic regulation of important pathways as well as provide a major source of variation in the process of speciation, the importance of epistasis for genomic selection in the context of plant breeding is still being debated. In this paper, we report the results on the prediction of genetic values with epistatic effects for 280 accessions in the Nebraska Wheat Breeding Program using adaptive mixed least absolute shrinkage and selection operator (LASSO). The development of adaptive mixed LASSO, originally designed for association mapping, for the context of genomic selection is reported. The results show that adaptive mixed LASSO can be successfully applied to the prediction of genetic values while incorporating both marker main effects and epistatic effects. Especially, the prediction accuracy is substantially improved by the inclusion of two-locus epistatic effects (more than onefold in some cases as measured by cross-validation correlation coefficient), which is observed for multiple traits and planting locations. This points to significant potential in using non-additive genetic effects for genomic selection in crop breeding practices.     

Long day plants and the response to global warming: rapid evolutionary change in day length sensitivity is possible in wild beet

Day length is a key factor in flowering induction in many plant species in a seasonal environment with flowering induction usually happening at shorter day lengths in lower latitudes. Now, the climate changes systematically at a considerable speed due to global warming. As a consequence, earlier flowering will be selected for in long day plants by favouring a lower threshold for day length sensitivity, on the condition of available genetic variability. Here, we show that there is considerable genetic variation for day length sensitivity in our study species, the seabeet Beta vulgaris subsp. maritima. In the northernmost natural populations without vernalization requirement, in southwest France, the necessary day length for flowering induction could be reduced by artificial selection in <10 generations from >13 h to <11 h, the latter value corresponding to populations in the Beta-species complex from Northern Africa and the eastern part of the Mediterranean tested under the same conditions. A quantitative genetic analysis provided evidence of a gradual change without detectable major genes. Additional experiments were carried out to separate the response to photoperiod from age and energy effects. A certain effect of energy availability has been found, whereas age effects could be excluded. These results indicate a considerable potential for evolutionary change in adjusting flowering time in a changing climate.     

Introduction. Integration of ecology and endocrinology in avian reproduction: a new synthesis

Birds are some of the most familiar organisms of global ecosystems. Changes in the visibility and abundance of birds are therefore excellent indicators of population and physiological responses to habitat changes and are a major focus for public concern about detrimental environmental changes. In order to understand how birds respond to these challenges, it is essential to determine how the environment affects reproduction under natural conditions. The continuum from environmental variables (cues) to reproductive life-history traits depends upon a cascade of neural and physiological processes that determine the extent and rate at which birds will be able to adapt to changes in their environment. For a full understanding of this ability to adapt, ecologists and endocrinologists need to collaborate and build a common framework. The objective of this theme issue is to bring together a series of papers addressing how evolutionary ecologists and endocrinologists can collaborate directly using avian reproduction as a model system. First, we address the need to integrate ecology and endocrinology and what benefits to biological knowledge will be gained. The papers collected in this issue represent a new synthesis of ecology and endocrinology as discussed in three E-BIRD workshops. The three main foci are trade-offs and constraints, maternal effects and individual variation. Authors within each group present ecological and endocrinological aspects of their topics and many go on to outline testable hypotheses. Finally, we discuss where the major problems remain and how this issue points out where these need collaborative efforts of ecologists and endocrinologists. Specific challenges are raised to future researchers to break through intellectual barriers and explore new frontiers. This framework of topics will ultimately apply to all taxa because the principles involved are universal and hopefully will have direct application to programmes integrating organisms and genes throughout biological sciences.     

The evolutionary ecology of individual phenotypic plasticity in wild populations

The ability of individual organisms to alter morphological and life-history traits in response to the conditions they experience is an example of phenotypic plasticity which is fundamental to any population's ability to deal with short-term environmental change. We currently know little about the prevalence, and evolutionary and ecological causes and consequences of variation in life history plasticity in the wild. Here we outline an analytical framework, utilizing the reaction norm concept and random regression statistical models, to assess the between-individual variation in life history plasticity that may underlie population level responses to the environment at both phenotypic and genetic levels. We discuss applications of this framework to date in wild vertebrate populations, and illustrate how natural selection and ecological constraint may alter a population's response to the environment through their effects at the individual level. Finally, we present future directions and challenges for research into individual plasticity.     

Selection on domestication traits and quantitative trait loci in crop–wild sunflower hybrids

The strength and extent of gene flow from crops into wild populations depends, in part, on the fitness of the crop alleles, as well as that of alleles at linked loci. Interest in crop–wild gene flow has increased with the advent of transgenic plants, but nontransgenic crop–wild hybrids can provide case studies to understand the factors influencing introgression, provided that the genetic architecture and the fitness effects of loci are known. This study used recombinant inbred lines (RILs) generated from a cross between crop and wild sunflowers to assess selection on domestication traits and quantitative trait loci (QTL) in two contrasting environments, in Indiana and Nebraska, USA. Only a small fraction of plants (9%) produced seed in Nebraska, due to adverse weather conditions, while the majority of plants (79%) in Indiana reproduced. Phenotypic selection analysis found that a mixture of crop and wild traits were favoured in Indiana (i.e. had significant selection gradients), including larger leaves, increased floral longevity, larger disk diameter, reduced ray flower size and smaller achene (seed) mass. Selection favouring early flowering was detected in Nebraska. QTLs for fitness were found at the end of linkage groups six (LG6) and nine (LG9) in both field sites, each explaining 11–12% of the total variation. Crop alleles were favoured on LG9, but wild alleles were favoured on LG6. QTLs for numerous domestication traits overlapped with the fitness QTLs, including flowering date, achene mass, head number, and disk diameter. It remains to be seen if these QTL clusters are the product of multiple linked genes, or individual genes with pleiotropic effects. These results indicate that crop trait values and alleles may sometimes be favoured in a noncrop environment and across broad geographical regions.     

A steep cline in ladybird melanism has decayed over 25 years: a genetic response to climate change?

A cline in the frequency of melanic morphs of the two-spot ladybird, Adalia bipunctata, was first surveyed in 1980 along a transect extending inland from the coast in the Netherlands. At that time, the frequency of melanics increased over some 40 km from 10% near the coast to nearly 60% inland. Additional surveys made in 1991 and 1995 demonstrated some progressive change in cline shape. New samples from 1998 and 2004 confirm these dynamics, and show that over a period of about 50 generations for the beetle, the cline had decayed rapidly to yield rather uniform frequencies of melanic morphs at around 20% along the whole transect by 2004. Climate data and evidence for thermal melanism in this species support our contention that these dynamics reflect a dramatic example of a rapid genetic response within populations to climate change and local selection.     

Strong artificial selection in the wild results in predicted small evolutionary change

Estimates of genetic variation and selection allow for quantitative predictions of evolutionary change, at least in controlled laboratory experiments. Natural populations are, however, different in many ways, and natural selection on heritable traits does not always result in phenotypic change. To test whether we were able to predict the evolutionary dynamics of a complex trait measured in a natural, heterogeneous environment, we performed, over an 8-year period, a two-way selection experiment on clutch size in a subdivided island population of great tits (Parus major). Despite strong artificial selection, there was no clear evidence for evolutionary change at the phenotypic level. Environmentally induced differences in clutch size among years are, however, large and can mask evolutionary changes. Indeed, genetic changes in clutch size, inferred from a statistical model, did not deviate systematically from those predicted. Although this shows that estimates of genetic variation and selection can indeed provide quantitative predictions of evolutionary change, also in the wild, it also emphasizes that demonstrating evolution in wild populations is difficult, and that the interpretation of phenotypic trends requires great care.     

Abiotic factors influencing the ecology of wild rabbit fleas in north-eastern Spain

During 1992, the population dynamics of rabbit fleas were compared at two sites in north-eastern Spain. The sites differed mainly in terms of annual rainfall and soil type. All flea species showed seasonal cycles of abundance, although peaks in numbers occurred at different times, reflecting their specific adaptations for coping with climatic variables. Adult Spilopsyllus cuniculi (Dale) (Siphonaptera: Pulicidae) were found largely parasitizing rabbits in spring and adult Caenopsylla laptevi (Beaucournu etal.) (Siphonaptera: Ceratophyllidae) in the autumn. In contrast, monthly flea indices of Xenopsylla cunicularis (Smit) (Siphonaptera: Pulicidae) and Echidnophaga iberica (Ribeiro et al.) (Siphonaptera: Pulicidae) peaked in summer. Spilopsyllus cuniculi was present at both sites, but was less common on the drier site, where monthly mean temperature and annual rainfall approached the flea's physiological limits. By contrast, E. iberica, X. cunicularis and C. laptevi, known to be better adapted for dryness, showed the opposite patterns of abundance. Nevertheless, even these arid-adapted species took advantage of the milder and wetter spring (X. cunicularis and E. iberica) or autumn (C. laptevi) for breeding and larval development. Although environmental temperature, rainfall and soil texture will influence the microclimate of the burrows where the flea larvae develop, burrow humidity seems to be more dependent on soil characteristics and past rainfall rather than the humidity of the external air.     

The evolution of quantitative traits in complex environments

Species inhabit complex environments and respond to selection imposed by numerous abiotic and biotic conditions that vary in both space and time. Environmental heterogeneity strongly influences trait evolution and patterns of adaptive population differentiation. For example, heterogeneity can favor local adaptation, or can promote the evolution of plastic genotypes that alter their phenotypes based on the conditions they encounter. Different abiotic and biotic agents of selection can act synergistically to either accelerate or constrain trait evolution. The environmental context has profound effects on quantitative genetic parameters. For instance, heritabilities measured in controlled conditions often exceed those measured in the field; thus, laboratory experiments could overestimate the potential for a population to respond to selection. Nevertheless, most studies of the genetic basis of ecologically relevant traits are conducted in simplified laboratory environments, which do not reflect the complexity of nature. Here, we advocate for manipulative field experiments in the native ranges of plant species that differ in mating system, life-history strategy and growth form. Field studies are vital to evaluate the roles of disparate agents of selection, to elucidate the targets of selection and to develop a nuanced perspective on the evolution of quantitative traits. Quantitative genetics field studies will also shed light on the potential for natural populations to adapt to novel climates in highly fragmented landscapes. Drawing from our experience with the ecological model system Boechera (Brassicaceae), we discuss advancements possible through dedicated field studies, highlight future research directions and examine the challenges associated with field studies.