Evolutionary Change In Response Research Articles

The Difficulty of Predicting Evolutionary Change in Response to Novel Ecological Interactions: A Field Experiment with Anolis Lizards.

AbstractDetermining whether and how evolution is predictable is an important goal, particularly as anthropogenic disturbances lead to novel species interactions that could modify selective pressures. Here, we use a multigeneration field experiment with brown anole lizards (Anolis sagrei) to test hypotheses about the predictability of evolution. We manipulated the presence/absence of predators and competitors of A. sagrei across 16 islands in the Bahamas that had preexisting brown anole populations. Before the experiment and again after roughly five generations, we measured traits related to locomotor performance and habitat use by brown anoles and used double-digest restriction enzyme-associated DNA sequencing to estimate genome-wide changes in allele frequencies. Although previous work showed that predators and competitors had characteristic effects on brown anole behavior, diet, and population sizes, we found that evolutionary change at both phenotypic and genomic levels was difficult to forecast. Phenotypic changes were contingent on sex and habitat use, whereas genetic change was unpredictable and not measurably correlated with phenotypic changes, experimental treatments, or other environmental factors. Our work shows how differences in ecological context can alter evolutionary outcomes over short timescales and underscores the difficulty of forecasting evolutionary responses to multispecies interactions in natural conditions, even in a well-studied system with ample supporting ecological information.

Infectious disease ecology and evolution in a changing world.

Infectious disease ecology and evolution in a changing world.

Rapid evolution of life-history traits in response to warming, predation and competition: A meta-analysis.

Although studies quantifying evolutionary change in response to the selective pressures that organisms face in the wild have demonstrated that organisms can evolve rapidly, we lack a systematic assessment of the frequency, magnitude and direction of rapid evolutionary change across taxa. To address this gap, we conducted a meta-analysis of 58 studies that document the effects of warming, predation or competition on the evolution of body size, development rate or fecundity in natural or experimental animal populations. We tested whether there was a consistent effect of any selective agent on any trait, whether the direction of these effects align with theoretical predictions, and whether the three agents select in opposing directions on any trait. Overall, we found weak effects of all three selective agents on trait evolution: none of our nine traits by selective agent combinations had an overall effect that differed from zero, only 31% of studies had a significant within-study effect, and attributes of the included studies generally did not account for between-study variation in results. One notable exception was that predation targeting adults consistently resulted in the evolution of smaller prey body size. We discuss potential causes of these generally weak responses and consider how our results inform the ongoing development of eco-evolutionary research.

Genomic evidence for parallel adaptation to cities.

Urban evolutionary biology is the study of rapid evolutionary change in response to humans and our uses of land to support city dwellers. Because cities are relatively modern additions to the natural world, research on urban evolution tends to focus on microevolutionary change that has happened across a few to many hundreds of generations. These questions still fall under the broad purview of evolutionary ecology. However, the severity, rapidity and replication of environmental changes that drive evolution in this context make it worthy of specific attention. Urban evolution provides the opportunity to study the earliest stages of evolution in a context that is scientifically interesting and societally important. The newness of urban populations and their proximity to natural populations also creates challenges when trying to detect population genetic change. In a From the Cover article in this issue of Molecular Ecology, Mueller et al. use whole genome resequencing data to address some of these challenges while exploring genetic changes associated with urbanization in three replicate urban-rural burrowing owl (Athene cunicularia) populations. Combining multiple approaches across these sample sites Mueller et al. find evidence for selection on genes whose function is related to synapses, neuron projections, brain connectivity and cognitive function in general. That selection was parallel suggests that phenotypes related to brain processes were probably particularly important for urban adaptation.

A century of intermittent eco-evolutionary feedbacks resulted in novel trait combinations in invasive Great Lakes alewives (Alosa pseudoharengus).

Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco‐evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large‐bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non‐native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present‐day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long‐distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations.

Reaction norm analysis reveals rapid shifts toward delayed maturation in harvested Lake Erie yellow perch (Perca flavescens).

Harvested marine fish stocks often show a rapid and substantial decline in the age and size at maturation. Such changes can arise from multiple processes including fisheries‐induced evolution, phenotypic plasticity, and responses to environmental factors other than harvest. The relative importance of these processes could differ systematically between marine and freshwater systems. We tested for temporal shifts in the mean and within‐cohort variability of age‐ and size‐based maturation probabilities of female yellow perch (Perca flavescens Mitchill) from four management units (MUs) in Lake Erie. Lake Erie yellow perch have been commercially harvested for more than a century, and age and size at maturation have varied since sampling began in the 1980s. Our analysis compared probabilistic maturation reaction norms (PMRNs) for cohorts when abundance was lower and harvest higher (1993–1998) to cohorts when abundance was higher and harvest lower (2005–2010). PMRNs have been used in previous studies to detect signs of evolutionary change in response to harvest. Maturation size threshold increased between the early and late cohorts, and the increases were statistically significant for the youngest age in the western MU1 and for older ages in the eastern MU3. Maturation envelope widths, a measure of the variability in maturation among individuals in a cohort, also increased between early and late cohorts in the western MUs where harvest was highest. The highest rates of change in size at maturation for a given age were as large or larger than rates reported for harvested marine fishes where declines in age and size at maturation have been observed. Contrary to the general observation of earlier maturation evolving in harvested stocks, female yellow perch in Lake Erie may be rapidly evolving delayed maturation since harvest was relaxed in the late 1990s, providing a rare example of possible evolutionary recovery.

Paternal‐effects in a terrestrial ectotherm are temperature dependent but no evidence for adaptive effects

Abstract Global rising of average temperatures and increase in extreme climatic events may largely impact animal survival and reproduction. Yet, how variation in temperature may affect male fertility, in particular ejaculate traits, and whether this can in turn affect offspring fitness, is seldom addressed. Paternal effects may be of key importance as they could impact the rate and direction of evolutionary change in response to climate change. We tested the effects of temperature experienced by males on sperm traits, and asked whether the paternal environmental temperature affected offspring phenotype. We further explored the potential for paternal effects to be adaptive, which would occur when offspring fitness increased under the same environmental conditions experienced by the fathers. We exposed male field crickets to high or low temperatures at two life stages, either throughout development or as adults, and tested sperm traits (number and quality) and offspring fitness (hatching success and survival). We further assessed sperm traits in offspring, after they had also been exposed to the same or different temperature experienced by their father. We found that temperature affected sperm traits depending on the life‐stage of individuals. When the exposure was given during adulthood, males exposed to high temperature produced less sperm and of lower quality compared to males exposed to lower temperature, while if exposure was given during development, males exposed to high temperature produced more sperm and of better quality compared to males exposed to low temperatures. Offspring fitness was significantly affected by paternal temperature, evidence for anticipatory paternal effects on sperm traits was not found. Our study indicates that temperature can mediate cross‐generational effects, and that paternal effects may be mediated by changes in temperature and therefore much more widespread in nature than previously assumed. A plain language summary is available for this article.

A Matter of Taste: Lineage-Specific Loss of Function of Taste Receptor Genes in Vertebrates.

Vertebrates can perceive at least five different taste qualities, each of which is thought to have a specific role in the evolution of different species. The avoidance of potentially poisonous foods, which are generally bitter or sour tasting, and the search for more nutritious ones, those with high-fat and high-sugar content, are two of the most well-known examples. The study of taste genes encoding receptors that recognize ligands triggering taste sensations has helped to reconstruct several evolutionary adaptations to dietary changes. In addition, an increasing number of studies have focused on pseudogenes, genomic DNA sequences that have traditionally been considered defunct relatives of functional genes mostly because of the presence of deleterious mutations interrupting their open reading frames. The study of taste receptor pseudogenes has helped to shed light on how the evolutionary history of taste in vertebrates has been the result of a succession of gene gain and loss processes. This dynamic role in evolution has been explained by the “less-is-more” hypothesis, suggesting gene loss as a mechanism of evolutionary change in response to a dietary shift. This mini-review aims at depicting the major lineage-specific loss of function of taste receptor genes in vertebrates, stressing their evolutionary importance and recapitulating signatures of natural selection and their correlations with food habits.

Evolution caused by extreme events.

Extreme events can be a major driver of evolutionary change over geological and contemporary timescales. Outstanding examples are evolutionary diversification following mass extinctions caused by extreme volcanism or asteroid impact. The evolution of organisms in contemporary time is typically viewed as a gradual and incremental process that results from genetic change, environmental perturbation or both. However, contemporary environments occasionally experience strong perturbations such as heat waves, floods, hurricanes, droughts and pest outbreaks. These extreme events set up strong selection pressures on organisms, and are small-scale analogues of the dramatic changes documented in the fossil record. Because extreme events are rare, almost by definition, they are difficult to study. So far most attention has been given to their ecological rather than to their evolutionary consequences. We review several case studies of contemporary evolution in response to two types of extreme environmental perturbations, episodic (pulse) or prolonged (press). Evolution is most likely to occur when extreme events alter community composition. We encourage investigators to be prepared for evolutionary change in response to rare events during long-term field studies.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'.

Synergism and Antagonism of Proximate Mechanisms Enable and Constrain the Response to Simultaneous Selection on Body Size and Development Time: An Empirical Test Using Experimental Evolution.

Natural selection acts on multiple traits simultaneously. How mechanisms underlying such traits enable or constrain their response to simultaneous selection is poorly understood. We show how antagonism and synergism among three traits at the developmental level enable or constrain evolutionary change in response to simultaneous selection on two focal traits at the phenotypic level. After 10 generations of 25% simultaneous directional selection on all four combinations of body size and development time in Manduca sexta (Sphingidae), the changes in the three developmental traits predict 93% of the response of development time and 100% of the response of body size. When the two focal traits were under synergistic selection, the response to simultaneous selection was enabled by juvenile hormone and ecdysteroids and constrained by growth rate. When the two focal traits were under antagonistic selection, the response to selection was due primarily to change in growth rate and constrained by the two hormonal traits. The approach used here reduces the complexity of the developmental and endocrine mechanisms to three proxy traits. This generates explicit predictions for the evolutionary response to selection that are based on biologically informed mechanisms. This approach has broad applicability to a diverse range of taxa, including algae, plants, amphibians, mammals, and insects.

Transition to annual life history coincides with reduction in cell cycle speed during early cleavage in three independent clades of annual killifish.

BackgroundAnnual killifishes inhabit temporary ponds and their embryos survive the dry season encased in the mud by entering diapause, a process that arrests embryonic development during hostile conditions. Annual killifishes are present within three clades distributed in Africa (one East and one West of the Dahomey gap) and South America. Within each of these phylogenetic clades, a non-annual clade is sister taxon to a annual clade and therefore represent an example of convergent evolution.Early cleavage of teleost embryos is characterized by a very fast cell cycle (15-30 minutes) and lack of G1 and G2 phases. Here, we decided to investigate rates of early cleavage in annual killifishes. In addition, we specifically tested whether also annual killifish embryos lack G1 and G2 phases.ResultsWe used time lapse brightfield microscopy to investigate cell division kinetics during the first developmental stages of annual- and non-annual species belonging to the three different phylogenetic clades. Annual killifishes of all three clades showed cleavage times significantly longer when compared to their non-annual sister taxa (average 35 min vs. average 75 min). Using FUCCI fluorescent imaging of the cell cycle after microinjection in the annual species Nothobranchius furzeri, we demonstrate that the first 5 division are synchronous and do not show a G1 phase. Cell cycle synchronization is lost after the 5th cleavage division.ConclusionsOur results show, for the first time, that cell cycle rate during cleavage, a trait thought to be rather evolutionary conserved can undergo convergent evolutionary change in response to variations in life-history.

An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population.

Glucocorticoid hormones (CORT) are predicted to promote adaptation to variable environments, yet little is known about the potential for CORT secretion patterns to respond to selection in free-living populations. We assessed the heritable variation underlying differences in hormonal phenotypes using a cross-foster experimental design with nestling North American barn swallows (Hirundo rustica erythrogaster). Using a bivariate animal model, we partitioned variance in baseline and stress-induced CORT concentrations into their additive genetic and rearing environment components and estimated their genetic correlation. Both baseline and stress-induced CORT were heritable with heritability of 0.152 and 0.343, respectively. We found that the variation in baseline CORT was best explained by rearing environment, whereas the variation in stress-induced CORT was contributed to by a combination of genetic and environmental factors. Further, we did not detect a genetic correlation between these two hormonal traits. Although rearing environment appears to play an important role in the secretion of both types of CORT, our results suggest that stress-induced CORT levels are underlain by greater additive genetic variance compared with baseline CORT levels. Accordingly, we infer that the glucocorticoid response to stress has a greater potential for evolutionary change in response to selection compared with baseline glucocorticoid secretion patterns.

The genetic covariance between life cycle stages separated by metamorphosis.

Metamorphosis is common in animals, yet the genetic associations between life cycle stages are poorly understood. Given the radical changes that occur at metamorphosis, selection may differ before and after metamorphosis, and the extent that genetic associations between pre- and post-metamorphic traits constrain evolutionary change is a subject of considerable interest. In some instances, metamorphosis may allow the genetic decoupling of life cycle stages, whereas in others, metamorphosis could allow complementary responses to selection across the life cycle. Using a diallel breeding design, we measured viability at four ontogenetic stages (embryo, larval, juvenile and adult viability), in the ascidian Ciona intestinalis and examined the orientation of additive genetic variation with respect to the metamorphic boundary. We found support for one eigenvector of G: (gobsmax ), which contrasted larval viability against embryo viability and juvenile viability. Target matrix rotation confirmed that while gobsmax shows genetic associations can extend beyond metamorphosis, there is still considerable scope for decoupled phenotypic evolution. Therefore, although genetic associations across metamorphosis could limit that range of phenotypes that are attainable, traits on either side of the metamorphic boundary are capable of some independent evolutionary change in response to the divergent conditions encountered during each life cycle stage.

Meta‐analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA)

Ecological explanations for the success and persistence of invasive species vastly outnumber evolutionary hypotheses, yet evolution is a fundamental process in the success of any species. The Evolution of Increased Competitive Ability (EICA) hypothesis (Blossey and Nötzold 1995) proposes that evolutionary change in response to release from coevolved herbivores is responsible for the success of many invasive plant species. Studies that evaluate this hypothesis have used different approaches to test whether invasive populations allocate fewer resources to defense and more to growth and competitive ability than do source populations, with mixed results. We conducted a meta-analysis of experimental tests of evolutionary change in the context of EICA. In contrast to previous reviews, there was no support across invasive species for EICA's predictions regarding defense or competitive ability, although invasive populations were more productive than conspecific native populations under noncompetitive conditions. We found broad support for genetically based changes in defense and competitive plant traits after introduction into new ranges, but not in the manner suggested by EICA. This review suggests that evolution occurs as a result of plant introduction and population expansion in invasive plant species, and may contribute to the invasiveness and persistence of some introduced species.

Response to enemies in the invasive plant Lythrum salicaria is genetically determined

The enemy release hypothesis assumes that invasive plants lose their co-evolved natural enemies during introduction into the new range. This study tested, as proposed by the evolution of increased competitive ability (EICA) hypothesis, whether escape from enemies results in a decrease in defence ability in plants from the invaded range. Two straightforward aspects of the EICA are examined: (1) if invasives have lost their enemies and their defence, they should be more negatively affected by their full natural pre-invasion herbivore spectrum than their native conspecifics; and (2) the genetic basis of evolutionary change in response to enemy release in the invasive range has not been taken sufficiently into account. Lythrum salicaria (purple loosestrife) from several populations in its native (Europe) and invasive range (North America) was exposed to all above-ground herbivores in replicated natural populations in the native range. The experiment was performed both with plants raised from field-collected seeds as well as with offspring of these where maternal effects were removed. Absolute and relative leaf damage was higher for introduced than for native plants. Despite having smaller height growth rate, invasive plants attained a much larger final size than natives irrespective of damage, indicating large tolerance rather than effective defence. Origin effects on response to herbivory and growth were stronger in second-generation plants, suggesting that invasive potential through enemy release has a genetic basis. The findings support two predictions of the EICA hypothesis - a genetically determined difference between native and invasive plants in plant vigour and response to enemies - and point to the importance of experiments that control for maternal effects and include the entire spectrum of native range enemies.

A Flurry of Folding Problems: An Interview with Susan Lindquist

Susan Lindquist and I had been trying to intersect for an interview for about 5 years. Lindquist (Image 1), who is currently on the faculty at MIT's Whitehead Institute, is well-known for her work on protein chaperones and stress responses. Her interests grew out of thesis research in the early 1970s in Matt Meselson's lab, where she developed a strategy to study the heat-shock response in cultured cells of Drosophila, an approach that complemented observations on transcriptional puffs on polytene chromosomes. In the subsequent 20 years at the University of Chicago, Susan continued to pursue the biochemical and cell-biological properties of heat-shock proteins (HSPs), which assist with a host of protein-folding problems. In 1994, she found herself immersed in a mystery of non-Mendelian inheritance when Yury Chernoff called to say that one such protein, Hsp104, controlled the [PSI+] phenotype. This swept her from stress tolerance to prions and then on to problems of protein folding in cancer and neurodegeneration. I was eager to understand Susan's work and gain her perspective on how chaperones and remodeling proteins promote rapid evolutionary change in response to environmental stresses, a neo-Lamarkian view of biology.

Inheritance of nesting behaviour across natural environmental variation in a turtle with temperature-dependent sex determination

Nesting behaviour is critical for reproductive success in oviparous organisms with no parental care. In organisms where sex is determined by incubation temperature, nesting behaviour may be a prime target of selection in response to unbalanced sex ratios. To produce an evolutionary change in response to sex-ratio selection, components of nesting behaviour must be heritable. We estimated the field heritability of two key components of nesting behaviour in a population of painted turtles (Chrysemys picta) with temperature-dependent sex determination by applying the 'animal model' to a pedigree reconstructed from genotype data. We obtained estimates of low to non-detectable heritability using repeated records across all environments. We then determined environment-specific heritability by grouping records with similar temperatures for the winter preceding the nesting season, a variable known to be highly associated with our two traits of interest, nest vegetation cover and Julian date of nesting. The heritability estimates of nest vegetation cover and Julian date of nesting were qualitatively highest and significant, or nearly so, after hot winters. Additive genetic variance for these traits was not detectable after cold winters. Our analysis suggests that the potential for evolutionary change of nesting behaviour may be dependent on the thermal conditions of the preceding winter, a season that is predicted to be especially subject to climate change.

Pollen-tube growth rates in Collinsia heterophylla (Plantaginaceae): one-donor crosses reveal heritability but no effect on sporophytic-offspring fitness

Evolutionary change in response to natural selection will occur only if a trait confers a selective advantage and there is heritable variation. Positive connections between pollen traits and fitness have been found, but few studies of heritability have been conducted, and they have yielded conflicting results. To understand better the evolutionary significance of pollen competition and its potential role in sexual selection, the heritability of pollen tube-growth rate and the relationship between this trait and sporophytic offspring fitness were investigated in Collinsia heterophylla. Because the question being asked was if female function benefited from obtaining genetically superior fathers by enhancing pollen competition, one-donor (per flower) crosses were used in order to exclude confounding effects of post-fertilization competition/allocation caused by multiple paternity. Each recipient plant was crossed with an average of five pollen donors. Pollen-tube growth rate and sporophytic traits were measured in both generations. Pollen-tube growth rate in vitro differed among donors, and the differences were correlated with in vivo growth rate averaged over two to four maternal plants. Pollen-tube growth rate showed significant narrow-sense heritability and evolvability in a father-offspring regression. However, this pollen trait did not correlate significantly with sporophytic-offspring fitness. These results suggest that pollen-tube growth rate can respond to selection via male function. The data presented here do not provide any support for the hypothesis that intense pollen competition enhances maternal plant fitness through increased paternity by higher-quality sporophytic fathers, although this advantage cannot be ruled out. These data are, however, consistent with the hypothesis that pollen competition is itself selectively advantageous, through both male and female function, by reducing the genetic load among successful gametophytic fathers (pollen), and reducing inbreeding depression associated with self-pollination in plants with mix-mating systems.

Evolutionary concepts in predicting and evaluating the impact of mass chemotherapy schistosomiasis control programmes on parasites and their hosts.

SummarySchistosomiasis is a parasitic disease of significant medical and veterinary importance in many regions of the world. Recent shifts in global health policy have led towards the implementation of mass chemotherapeutic control programmes at the national scale in previously ‘neglected’ countries such as those within sub-Saharan Africa. Evolutionary theory has an important role to play in the design, application and interpretation of such programmes. Whilst celebrating the rapid success achieved to date by such programmes, in terms of reduced infection prevalence, intensity and associated human morbidity, evolutionary change in response to drug selection pressure may be predicted under certain circumstances, particularly in terms of the development of potential drug resistance, evolutionary changes in parasite virulence, transmission and host use, and/or competitive interactions with co-infecting pathogens. Theoretical and empirical data gained to date serve to highlight the importance of careful monitoring and evaluation of parasites and their hosts whenever and wherever chemotherapy is applied and where parasite transmission remains.

Evolutionary response to size-selective mortality in an exploited fish population

Many collapsed fish populations have failed to recover after a decade or more with little fishing. This may reflect evolutionary change in response to the highly selective mortality imposed by fisheries. Recent experimental work has demonstrated a rapid genetic change in growth rate in response to size-selective harvesting of laboratory fish populations. Here, we use a 30-year time-series of back-calculated lengths-at-age to test for a genetic response to size-selective mortality in the wild in a heavily exploited population of Atlantic cod (Gadus morhua). Controlling for the effects of density- and temperature-dependent growth, the change in mean length of 4-year-old cod between offspring and their parental cohorts was positively correlated with the estimated selection differential experienced by the parental cohorts between this age and spawning. This result supports the hypothesis that there have been genetic changes in growth in this population in response to size-selective fishing. Such changes may account for the continued small size-at-age in this population despite good conditions for growth and little fishing for over a decade. This study highlights the need for management regimes that take into account the evolutionary consequences of fishing.