Severe Fitness Consequences Research Articles

Quantitative disease resistance in wild Silene vulgaris to its endemic pathogen Microbotryum silenes-inflatae.

The evolution of disease resistances is an expected feature of plant-pathogen systems, but whether the genetics of this trait most often produces qualitative or quantitative phenotypic variation is a significant gap in our understanding of natural populations. These two forms of resistance variation are often associated with differences in number of underlying loci, the specificities of host-pathogen coevolution, as well as contrasting mechanisms of preventing or slowing the infection process. Anther-smut disease is a commonly studied model for disease of wild species, where infection has severe fitness impacts, and prior studies have suggested resistance variation in several host species. However, because the outcome of exposing the individual host to this pathogen is binary (healthy or diseased), resistance has been previously measured at the family level, as the proportion of siblings that become diseased. This leaves uncertain whether among-family variation reflects contrasting ratios of segregating discrete phenotypes or continuous trait variation among individuals. In the host Silene vulgaris, plants were replicated by vegetative propagation in order to quantify the infection rates of the individual genotype with the endemic anther-smut pathogen, Microbotryum silenes-inflatae. The variance among field-collected families for disease resistance was significant, while there was unimodal continuous variation in resistance among genotypes. Using crosses between genotypes within ranked resistance quartiles, the offspring infection rate was predicted by the parental resistance values. While the potential remains in this system for resistance genes having major effects, as there were suggestions of such qualitative resistance in a prior study, here the quantitative disease resistance to the endemic anther-smut pathogen is indicated for S. vulgaris. The variation in natural populations and strong heritability of the trait, combined with severe fitness consequences of anther-smut disease, suggests that resistance in these host populations is highly capable of responding to disease-induced selection.

Extremely low seasonal prey capture efficiency in a deep-diving whale, the narwhal.

Successful foraging is essential for individuals to maintain the positive energy balance required for survival and reproduction. Yet, prey capture efficiency is poorly documented in marine apex predators, especially deep-diving mammals. We deployed acoustic tags and stomach temperature pills in summer to collect concurrent information on presumed foraging activity (through buzz detection) and successful prey captures (through drops in stomach temperature), providing estimates of feeding efficiency in narwhals. Compared to the daily number of buzzes (707 ± 368), the daily rate of feeding events was particularly low in summer (19.8 ± 8.9) and only 8-14% of the foraging dives were successful (i.e. with a detectable prey capture). This extremely low success rate resulted in a very low daily food consumption rate (less than 0.5% of body mass), suggesting that narwhals rely on body reserves accumulated in winter to sustain year-round activities. The expected changes or disappearance of their wintering habitats in response to climate change may therefore have severe fitness consequences for narwhal populations.

An assessment of hybridization potential between Atlantic and Pacific salmon

Salmonids possess straying abilities that allows them to exploit open territory and establish new populations. Atlantic salmon (Salmo salar) are expanding their distribution primarily as first-generation escapes from aquaculture, whereas Pacific salmon (Oncorhynchus spp.) are expanding their range in polar and temperate regions due to both anthropogenic and natural influences. Here we utilize artificial intergeneric reciprocal crosses to assess the ability of seven species of Pacific salmon to hybridize with Atlantic salmon. Most cross types were found to produce low numbers of hatched embryos, but none survived to sexual maturation. Survivors consisted of diploids and triploids containing both Atlantic and Pacific salmon parental genomes. Thus, introgression of DNA between Pacific and Atlantic salmon may occur to form F1 hybrids, but transmission to subsequent generations is expected to be rare and occur only over evolutionary time scales. Further, the low viability observed for the most part at early stages of development and in both reciprocal crosses indicates that intergeneric crosses in nature between Atlantic and Pacific salmon are expected to have severe fitness consequences for both dams and sires.

Color of Artificial Light at Night Affects Incubation Behavior in the Great Tit, Parus major

Artificial light at night (ALAN) has been recognized as a biodiversity threat due to the drastic effects it can have on many organisms. In wild birds, artificial illumination alters many natural behaviors that are important for fitness, including chick provisioning. Although incubation is a key determinant of the early developmental environment, studies into the effects of ALAN on bird incubation behavior are lacking. We measured nest temperature in nest boxes of great tits during the incubation period in two consecutive years. Nest boxes were located in eight previously dark field sites that have been experimentally illuminated since 2012 with white, green, or red light, or were left dark. We tested if light treatment affected mean nest temperature, number of times birds leave the nest (off-bout frequency), and off-bout duration during the incubation period. Subsequently, we investigated if incubation behavior is related to fitness. We found that birds incubating in the white light during a cold, early spring had lower mean nest temperatures at the end of incubation, both during the day and during the night, compared to birds in the green light. Moreover, birds incubating in white light took fewer off-bouts, but off-bouts were on average longer. The opposite was true for birds breeding in the green light. Low incubation temperatures and few but long off-bouts can have severe consequences for developing embryos. In our study, eggs from birds that took on average few off-bouts needed more incubation days to hatch compared to eggs from birds that took many off-bouts. Nevertheless, we found no clear fitness effects of light treatment or incubation behavior on the number of hatchlings or hatchling weight. Our results add to the growing body of literature that shows that effects of ALAN can be subtle, can differ due to the spectral composition of light, and can be year-dependent. These subtle alterations of natural behaviors might not have severe fitness consequences in the short-term. However, in the long term they could add up, negatively affecting parent condition and survival as well as offspring recruitment, especially in urban environments where more environmental pollutants are present.

A sliver of the past: The decimation of the genetic diversity of the Mexican wolf.

The endangered Mexican wolf (Canis lupus baileyi) is known to carry exceedingly low levels of genetic diversity. This could be (i) the result of long-term evolutionary patterns as they exist at the southernmost limit of the species distribution at a relatively reduced effective size, or (ii) due to rapid population decline caused by human persecution over the last century. If the former, purifying selection is expected to have minimized the impact of inbreeding. If the latter, rapid and recent declines in genetic diversity may have resulted in severe fitness consequences. To differentiate these hypotheses, we conducted comparative whole-genome analyses of five historical Mexican wolves (1907-1917) and 18 contemporary Mexican and grey wolves from North America and Eurasia. Based on whole-genome data, historical and modern Mexican wolves together form a discrete unit. Moreover, we found that modern Mexican wolves have reduced genetic diversity and increased inbreeding relative to the historical population, which was widespread across the southwestern United States and not restricted to Mexico as previously assumed. Finally, although Mexican wolves have evolved in sympatry with coyotes (C. latrans), we observed lower introgression between historical Mexican wolves and coyotes than with modern Mexican wolves, despite similarities in body size. Taken together, our data show that recent population declines probably caused the reduced level of genetic diversity, but not the observed differentiation of the Mexican wolves from other North American wolves.

Ultra-High Foraging Rates of Harbor Porpoises Make Them Vulnerable to Anthropogenic Disturbance

The question of how individuals acquire and allocate resources to maximize fitness is central in evolutionary ecology. Basic information on prey selection, search effort, and capture rates are critical for understanding a predator's role in its ecosystem and for predicting its response to natural and anthropogenic disturbance. Yet, for most marine species, foraging interactions cannot be observed directly. The high costs of thermoregulation in water require that small marine mammals have elevated energy intakes compared to similar-sized terrestrial mammals [1]. The combination of high food requirements and their position at the apex of most marine food webs may make small marine mammals particularly vulnerable to changes within the ecosystem [2-4], but the lack of detailed information about their foraging behavior often precludes an informed conservation effort. Here, we use high-resolution movement and prey echo recording tags on five wild harbor porpoises to examine foraging interactions in one of the most metabolically challenged cetacean species. We report that porpoises forage nearly continuously day and night, attempting to capture up to 550 small (3-10cm) fish prey per hour with a remarkable prey capture success rate of >90%. Porpoises therefore target fish that are smaller than those of commercial interest, but must forage almost continually to meet their metabolic demands with such small prey, leaving little margin for compensation. Thus, for these "aquatic shrews," even a moderate level of anthropogenic disturbance in the busy shallow waters they share with humans may have severe fitness consequences at individual and population levels.

Modeling winter moth Operophtera brumata egg phenology: nonlinear effects of temperature and developmental stage on developmental rate

Understanding the relationship between an insect's developmental rate and temperature is crucial to forecast insect phenology under climate change. In the winter moth Operophtera brumata timing of egg‐hatching has severe fitness consequences on growth and reproduction as egg‐hatching has to match bud burst of the host tree. In the winter moth, as in many insect species, egg development is strongly affected by ambient temperatures. Here we use laboratory experiments to show for the first time that the effect of temperature on developmental rate depends on the stage of development of the eggs. Building on this experimental finding, we present a novel physiological model to describe winter moth egg development in response to temperature. Our model, a modification of the existing Sharpe−Schoolfield biophysical model, incorporates the effect of developmental stage on developmental rate. Next we validate this model using a 13‐year data‐set from winter moth eggs kept under ambient conditions and compared this validation with a degree day model and with the Sharpe−Schoolfield model, which lacks the interaction between temperature and developmental stage on developmental rate. We show that accounting for the interaction between temperature and developmental stage improved the predictive power of the model and contributed to our understanding of annual variation in winter moth egg phenology. As climate change leads to unequal changes in temperatures throughout the year, a description of insect development in response to realistic patterns of temperature rather than an invariable degree‐day approach will help us to better predict future responses of insect phenology, and thereby insect fitness, to climate change.

Transgenerational phenotypic plasticity links breeding phenology with offspring life‐history

The timing of seasonal life‐history events is assumed to evolve to synchronize life cycles with the availability of resources. Temporal variation in breeding time can have severe fitness consequences for the offspring, but the interplay between adult reproductive decisions and offspring phenotypes remains poorly understood. Transgenerational plasticity (TGP) is a potential mechanism allowing rapid responses to environmental change. Here, we investigated if experimentally delayed breeding induces TGP in larval life‐history traits in the moor frog (Rana arvalis). We found clear evidence of TGP in response to changes in breeding phenology: delayed breeding increased offspring development and growth rates in the absence of external cues. This constitutes the first unequivocal evidence for TGP in response to changes in breeding phenology in vertebrates. TGP can play an important role in adjusting offspring life‐history strategies to the environment they are most likely to encounter, and may constitute an important mechanism for coping with climate change.

Detection of HIV-1 matrix protein p17 quasispecies variants in plasma of chronic HIV-1-infected patients by ultra-deep pyrosequencing.

The HIV-1 matrix protein p17 (p17MA) is a pleiotropic protein that plays a key role in the HIV-1 life cycle. It has been long believed to have a highly conserved primary amino acid sequence and a well-preserved structural integrity to avoid severe fitness consequences. However, recent data revealed that the carboxy (COOH)-terminus of p17MA possesses high levels of predicted intrinsic disorder, which would subtend to at least partially unfolded status of this region. This finding pointed to the need of investigating p17MA heterogeneity. The degree of intrapatient variations in the p17MA primary sequence was assessed on plasma viral RNA by using ultra-deep pyrosequencing. Data obtained support a complex nature of p17MA quasispecies, with variants present at variable frequency virtually in all patients. Clusters of mutations were scattered along the entire sequence of the viral protein, but they were more frequently detected within the COOH-terminal region of p17MA. Moreover, deletions and insertions also occurred in a restricted area of the COOH-terminal region. On the whole, our data show that the intrapatient level of sequence diversity in the p17MA is much higher than predicted before. Our results pave the way for further studies aimed at unraveling possible correlations between the presence of distinct p17MA variants and peculiar clinical evolutions of HIV-1 disease. The presence of p17MA quasispecies diversity may offer new tools to improve our understanding of the viral adaptation during the natural history of HIV-1 infection.

The effects of 17α-ethinyloestradiol on boldness and its relationship to decision making in male Siamese fighting fish

Behavioural syndromes have received much attention by behavioural ecologists in recent years. While the relationship between boldness across contexts and between boldness and aggression are frequently investigated, little is known about how these relationships might change because of environmental disturbances such as exposure to endocrine disrupters. 17α-ethinyloestradiol (EE2) is an oestrogen mimic that is prevalent in aquatic ecosystems worldwide and has severe, negative impacts on the behaviour and physiology of exposed organisms. To assess how EE2 affects boldness and decision making, male Siamese fighting fish, Betta splendens, received repeated trials of three boldness assays (novel environment, empty tank and novel object) and one decision-making assay (a dummy male and female presented simultaneously) before and after exposure to acute, nominal doses of EE2. A control group of males received the same number of trials but was not exposed to EE2. When subjects were unexposed, a behavioural syndrome was found for boldness across contexts. In addition, boldness was positively correlated with aggression in the decision-making context. EE2 exposure disrupted this behavioural syndrome. In summary, EE2 exposure reduced overall behavioural response in all contexts, disrupted the behavioural syndrome and reduced behavioural consistency. Thus, even nominal, short-term exposure to EE2 can have dramatic effects on multiple levels of behaviour and potentially generate severe fitness consequences on exposed aquatic species. This study provides the first evidence of a boldness–aggression syndrome in this species and demonstrates that pollution may negatively influence consistent individual differences in behaviour.

Predation risk causes oxidative damage in prey

While there is increasing interest in non-consumptive effects of predators on prey, physiological effects are understudied. While physiological stress responses play a crucial role in preparing escape responses, the increased metabolic rates and shunting of energy away from other body functions, including antioxidant defence, may generate costs in terms of increased oxidative stress. Here, we test whether predation risk increases oxidative damage in Enallagma cyathigerum damselfly larvae. Under predation risk, larvae showed higher lipid peroxidation, which was associated with lower levels of superoxide dismutase, a major antioxidant enzyme in insects, and higher superoxide anion concentrations, a potent reactive oxygen species. The mechanisms underlying oxidative damage are likely to be due to the shunting of energy away from antioxidant defence and to an increased metabolic rate, suggesting that the observed increased oxidative damage under predation risk may be widespread. Given the potentially severe fitness consequences of oxidative damage, this largely overlooked non-consumptive effect of predators may be contributing significantly to prey population dynamics.

Can terrestrial ectotherms escape the heat of climate change by moving?

Whether movement will enable organisms to alleviate thermal stress is central to the biodiversity implications of climate change. We use the temperature-dependence of ectotherm performance to investigate the fitness consequences of movement. Movement to an optimal location within a 50 km radius will only offset the fitness impacts of climate change by 2100 in 5 per cent of locations globally. Random movement carries an 87 per cent risk of further fitness detriment. Mountainous regions with high temperature seasonality (i.e. temperate areas) not only offer the greatest benefit from optimal movement but also the most severe fitness consequences if an organism moves to the wrong location. Doubling dispersal capacity would provide modest benefit exclusively to directed dispersers in topographically diverse areas. The benefits of movement for escaping climate change are particularly limited in the tropics, where fitness impacts will be most severe. The potential of movement to lessen climate change impacts may have been overestimated.

Revealing mechanisms underlying variation in malaria virulence: effective propagation and host control of uninfected red blood cell supply

Malaria parasite clones with the highest transmission rates to mosquitoes also tend to induce the most severe fitness consequences (or virulence) in mammals. This is in accord with expectations from the virulence–transmission trade-off hypothesis. However, the mechanisms underlying how different clones cause virulence are not well understood. Here, using data from eight murine malaria clones, we apply recently developed statistical methods to infer differences in clone characteristics, including induction of differing host-mediated changes in red blood cell (RBC) supply. Our results indicate that the within-host mechanisms underlying similar levels of virulence are variable and that killing of uninfected RBCs by immune effectors and/or retention of RBCs in the spleen may ultimately reduce virulence. Furthermore, the correlation between clone virulence and the degree of host-induced mortality of uninfected RBCs indicates that hosts increasingly restrict their RBC supply with increasing intrinsic virulence of the clone with which they are infected. Our results demonstrate a role for self-harm in self-defence for hosts and highlight the diversity and modes of virulence of malaria.

The role of genetic relatedness among social mates in a cooperative breeder

Breeding with relatives can have severe fitness consequences, so avoiding these costs is often evolutionarily favored. There are a number of mechanisms that reduce the likelihood of mating with relatives, including avoiding relatives as mates (through sexbiased dispersal and mate choice) and delayed sexual maturity in the presence of relatives. Here, we examine these mechanisms in Neolamprologus pulcher, a group-living cichlid fish that exhibits male-biased dispersal. Despite sex-biased dispersal in this species, mean relatedness between social mates was not different from that expected if pairs had formed randomly, suggesting individuals neither actively avoid nor prefer pairing with relatives. Furthermore, gonadal investment of subordinates living in social groups was not correlated with their relatedness to the opposite-sex dominant breeder in the group, suggesting that sexual maturation does not depend on the presence or absence of a relative. Highly related social pairs showed higher rates of within-pair aggression and lower rates of nonaggressive social affiliation than less-related social pairs. Breeder investment and indicators of female breeder and group quality were not correlated with relatedness values between social mates. However, scraping rates (a potential quality indicator) were lower in males paired with more closely related females. We consider whether the apparent lack of inbreeding avoidance reflects an evolutionary history of limited breeding opportunities in N. pulcher or a facultative strategy of more-fit individuals and discuss the behavioral results in light of the suggested nonassortative mating with regard to relatedness.

Multilocus heterozygosity and inbreeding depression in an insular house sparrow metapopulation

Inbreeding causes reduction of genetic variability that may have severe fitness consequences. In spite of its potentially huge impact on viability and evolutionary processes especially in small populations, quantitative demonstrations of genetic and demographic effects of inbreeding in natural populations are few. Here, we examine the relationship between individual inbreeding coefficients (F) and individual standardized multilocus heterozygosity (H) in an insular metapopulation of house sparrows (Passer domesticus) in northern Norway in order to evaluate whether H is a good predictor for F. We then relate variation in fitness (i.e. the probability of surviving from fledging to recruitment) to F and H, which enables us to examine whether inbreeding depression is associated with a reduction in genetic variability. The average level of inbreeding in the house sparrow metapopulation was high, and there was large inter-individual variation in F. As expected, standardized multilocus heterozygosity decreased with the level of inbreeding. The probability of recruitment was significantly negatively related to F, and, accordingly, increased with H. However, H explained no significant additional variation in recruitment rate than was explained by F. This suggests that H is a good predictor for F in this metapopulation, and that an increase in F is likely to be associated with a general increase in the level of homozygosity on loci across the genome, which has severe fitness consequences.

Phenology of Forest Caterpillars and Their Host Trees: The Importance of Synchrony

For many leaf-feeding herbivores, synchrony in phenology with their host plant is crucial as development outside a narrow phenological time window has severe fitness consequences. In this review, we link mechanisms, adaptation, and population dynamics within a single conceptual framework, needed for a full understanding of the causes and consequences of this synchrony. The physiological mechanisms underlying herbivore and plant phenology are affected by environmental cues, such as photoperiod and temperature, although not necessarily in the same way. That these different mechanisms lead to synchrony, even if there is spatial and temporal variation in plant phenology, is a result of the strong natural selection acting on the mechanism underlying herbivore phenology. Synchrony has a major impact on the population densities of leaf-feeding Lepidoptera, and years with a high synchrony may lead to outbreaks. Global climate change leads to a disruption of the synchrony between herbivores and their host plants, which may have major impacts for population viability if natural selection is insufficient to restore synchrony.

INFECTION SUCCESS IN NOVEL HOSTS: AN EXPERIMENTAL AND PHYLOGENETIC STUDY OF DROSOPHILA-PARASITIC NEMATODES

Surprisingly little is known about what determines a parasite's host range, which is essential in enabling us to predict the fate of novel infections. In this study, we evaluate the importance of both host and parasite phylogeny in determining the ability of parasites to infect novel host species. Using experimental lab assays, we infected 24 taxonomically diverse species of Drosophila flies (Diptera: Drosophilidae) with five different nematode species (Tylenchida: Allantonematidae: Howardula, Parasitylenchus), and measured parasite infection success, growth, and effects on female host fecundity (i.e., virulence). These nematodes are obligate parasites of mushroom-feeding Drosophila, particularly quinaria and testacea group species, often with severe fitness consequences on their hosts. We show that the potential host ranges of the nematodes are much larger than their actual ranges, even for parasites with only one known host species in nature. Novel hosts that are distantly related from the native host are much less likely to be infected, but among more closely related hosts, there is much variation in susceptibility. Potential host ranges differ greatly between the related parasite species. All nematode species that successfully infected novel hosts produced infective juveniles in these hosts. Most novel infections did not result in significant reductions in the fecundity of female hosts, with one exception: the host specialist Parasitylenchus nearcticus sterilized all quinaria group hosts, only one of which is a host in nature. The large potential host ranges of these parasites, in combination with the high potential for host colonization due to shared mushroom breeding sites, explain the widespread host switching observed in comparisons of nematode and Drosophila phylogenies.

Sperm competitive ability and genetic relatedness in Drosophila melanogaster: similarity breeds contempt.

Offspring of close relatives often suffer severe fitness consequences. Previous studies have demonstrated that females, when given a choice, will choose to avoid mating with closely related males. But where opportunities for mate choice are limited or kin recognition is absent, precopulatory mechanisms may not work. In this case, either sex could reduce the risks of inbreeding through mechanisms that occur during or after copulation. During mating, males or females could commit fewer gametes when mating with a close relative. After mating, females could offset the effects of mating with a closely related male through cryptic choice. Few prior studies of sperm competition have examined the effect of genetic similarity, however, and what studies do exist have yielded equivocal results. In an effort to resolve this issue, we measured the outcome of sperm competition when female Drosophila melanogaster were mated to males of four different degrees of genetic relatedness and then to a standardized competitor. We provide the strongest evidence to date that sperm competitive ability is negatively correlated with relatedness, even after controlling for inbreeding depression.

SPERM COMPETITIVE ABILITY AND GENETIC RELATEDNESS IN DROSOPHILA MELANOGASTER: SIMILARITY BREEDS CONTEMPT

Offspring of close relatives often suffer severe fitness consequences. Previous studies have demonstrated that females, when given a choice, will choose to avoid mating with closely related males. But where opportunities for mate choice are limited or kin recognition is absent, precopulatory mechanisms may not work. In this case, either sex could reduce the risks of inbreeding through mechanisms that occur during or after copulation. During mating, males or females could commit fewer gametes when mating with a close relative. After mating, females could offset the effects of mating with a closely related male through cryptic choice. Few prior studies of sperm competition have examined the effect of genetic similarity, however, and what studies do exist have yielded equivocal results. In an effort to resolve this issue, we measured the outcome of sperm competition when female Drosophila melanogaster were mated to males of four different degrees of genetic relatedness and then to a standardized competitor. We provide the strongest evidence to date that sperm competitive ability is negatively correlated with relatedness, even after controlling for inbreeding depression.

A sexual conflict in collared flycatchers, Ficedula albicollis: early male moult reduces female fitness

A sexual conflict over levels of parental care occurs in most animals with biparental care, and studies of sexual differences in levels of parental care have usually focused on its intra-annual fitness consequences. We investigated inter-annual fitness consequences of a sexual difference in timing of feather replacement (moult) in collared flycatchers (Ficedula albicollis). In this study, males overlapped reproduction and moult more often than females, they also initiated their moult at an earlier stage of breeding than females. Females mated to males with a moult-breeding overlap had significantly lowered survival chances than females mated with males initiating moult after breeding. Furthermore, females mated with moulting males risked a lowered future fecundity in terms of a delayed start to breeding in the following season. However, early moulting males achieved a similar reproductive success as males initiating moult after breeding. Likewise, male survival probability to the following breeding season did not differ between early and late moulting individuals, nor was there any evidence that males gained or lost in future mating advantages by moulting early. These results show not only that a sexual conflict over timing of moult may operate, but also that it can impose severe fitness consequences, in terms of reduced future fecundity and survival probability, upon the 'losing' sex.