Lifetime Fitness Research Articles

Lifetime fitness and age‐related female ornament signalling: evidence for survival and fecundity selection in the pied flycatcher

Ornaments displayed by females have often been denied evolutionary interest due to their frequently reduced expression relative to males, habitually attributed to a genetic correlation between the sexes. We estimated annual and lifetime reproductive success of female pied flycatchers (Ficedula hypoleuca) and applied capture-mark-recapture models to analyse annual survival rates in relation to the patterns of expression (absence/presence) of an ornament displayed by all males and a fraction of females. Overall, the likelihood of expressing the ornament increased nonlinearly with female age and was due to within-individual variation, not to the selective appearance or disappearance of ornament-related expression of phenotypes in the population. Accordingly, expressing the forehead patch in a given year did not influence survival probability. However, those females expressing the ornament at early ages (1-2 years old) enjoyed survival advantages throughout lifetime. Although ornamented females had higher lifetime fecundity and fledging success, their yearly reproductive performance, in terms of fledging productivity, decreased as they aged so that, late in life, ornamented females reared fewer offspring than nonexpressing females of the same age. In addition, both strategies (expressing vs. not expressing the trait) returned similar fitness payoffs in terms of recruited offspring. Our results support the hypothesis that fecundity and survival selection are involved in the displaying of this 'male' ornament by females.

Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana

Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment-specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2-5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.

Suitability of different dairy cow types for an Alpine organic and low-input milk production system

The implementation of a seasonal, site adapted, pasture-based milk production system as applied in New Zealand and North Western Europe might be an alternative for the near future in Alpine regions. As in such a low-input system the fertility and secondary traits such as robustness against metabolic challenges of dairy cows is of crucial importance, it is questionable whether conventional dairy cow types, which were selected primarily for milk production under high-input conditions, are most suitable. Therefore the aim of this study was to compare two different genotypes concerning their suitability for an organic, low-input milk production system under Alpine conditions. Between 2008 and 2011 records from 91 lactations of Brown Swiss (BS) and a special strain of Holstein Friesian (HFL) were collected at an experimental organic dairy farm. The BS cows represented the average Austrian BS population and were primarily selected for high milk yield. HFL cows were for decades selected under low-input conditions and were primarily bred for lifetime performance and fitness. The dataset was analysed using multi-factorial statistical models. BS was superior for most milk production parameters, but not for milk yield per unit of metabolic body weight. HFL had a lower body weight throughout the lactation, but mobilised significantly less body reserves, indicating a shorter and less negative energy balance. Both breeds had similar total feed and energy intake, but HFL had a significantly higher feed intake per unit of metabolic body weight. Furthermore, HFL conceived earlier and had a significantly shorter calving interval and an overall superior reproductive performance. Due to this, HFL has some advantages over conventional BS if managed in a pasture based, low-input milk production system, especially when block calving is involved.

Student-Centered Physical Education on a Shoestring Budget

Nationwide, only 56% of students attended physical education class on one or more days per week, and only 33% of students attended physical education daily in 2009. Physical educators have the responsibility to create positive experiences in physical education, as well as to develop physical skills and feelings of self-efficacy in their students. The National Association for Sport and Physical Education guidelines for youths recommend that children get 60 minutes of daily physical activity and avoid long periods of inactivity. In order to achieve this, physical education programs need to do more to promote lifetime fitness activities and more physical activity outside of the school day. This article outlines how to transform a traditional physical education class into one that provides relevant opportunities for students to be active for a lifetime based on their needs and interests.

Are elder siblings helpers or competitors? Antagonistic fitness effects of sibling interactions in humans.

Determining the fitness consequences of sibling interactions is pivotal for understanding the evolution of family living, but studies investigating them across lifetime are lacking. We used a large demographic dataset on preindustrial humans from Finland to study the effect of elder siblings on key life-history traits. The presence of elder siblings improved the chances of younger siblings surviving to sexual maturity, suggesting that despite a competition for parental resources, they may help rearing their younger siblings. After reaching sexual maturity however, same-sex elder siblings' presence was associated with reduced reproductive success in the focal individual, indicating the existence of competition among same-sex siblings. Overall, lifetime fitness was reduced by same-sex elder siblings' presence and increased by opposite-sex elder siblings' presence. Our study shows opposite effects of sibling interactions depending on the life-history stage, and highlights the need for using long-term fitness measures to understand the selection pressures acting on sibling interactions.

Time Resolved FRET in the SR Ca-ATPase

We have detected structural dynamics of the sarcoplasmic reticulum Ca-ATPase (SERCA) using time-resolved fluorescence spectroscopy. The Ca-ATPase from fast-twitch skeletal muscle (SERCA1a isoform) was labeled with cyan fluorescent protein (CFP) at the N-terminus in the actuator domain (A) and fluorescein isothiocyanate (FITC) at Lys-515 in the nucleotide-binding domain (N). Time-resolved FRET was detected between CFP (donor in A domain) and FITC (acceptor in N domain) for SERCA in ligand-stabilized states, including calcium-free (E2), calcium-bound (E1), and actively-cycling phosphoenzyme (EP). Lifetime fitting and molecular modeling were used to interpret fluorescence decays, thereby identifying a dynamic distribution of structural states within the cytoplasmic headpiece of SERCA (i.e., A-N interdomain distance). FRET results were compared to distance predictions from x-ray crystallography. We propose a structural mechanism for ligand activation of SERCA. Acknowledgments: Spectroscopy was performed in the Biophysical Spectroscopy Center at the University of Minnesota, with assistance from Fluorescence Innovations, Inc. (Gregory Gillispie, President). This work was funded by NIH grants to DDT (R01 GM27906, P30 AR0507220, T32 AR007612).

Sigma virus and male reproductive success in Drosophila melanogaster

The risk of disease transmission can affect female mating rate, and thus sexual conflict. Furthermore, the interests of a sexually transmitted organism may align or diverge with those of either sex, potentially making the disease agent a third participant in the sexual arms race. In Drosophila melanogaster, where sexual conflict over female mating rate is well established, we investigated how a common, non-lethal virus (sigma virus) might affect this conflict. We gave uninfected females the opportunity to copulate twice in no-choice trials: either with two uninfected males, or with one male infected with sigma virus followed by an uninfected male. We assessed whether females respond behaviorally to male infection, determined whether male infection affects either female or male reproductive success, and measured offspring infection rates. Male infection status did not influence time to copulation, or time to re-mating. However, male infection did affect male reproductive success: first males sired a significantly greater proportion of offspring, as well as more total offspring, when they were infected with sigma virus. Thus viral infection may provide males an advantage in sperm competition, or, possibly, females may preferentially use infected sperm. We found no clear costs of infection in terms of offspring survival. Viral reproductive success (the number of infected offspring) was strongly correlated with male reproductive success. Further studies are needed to demonstrate whether virus-induced changes in reproductive success affect male and female lifetime fitness, and whether virus-induced changes are under male, female, or viral control.

The role of river flow in the migration of adult Atlantic salmon, Salmo salar, through estuaries and rivers

AbstractAn assumption of Atlantic salmon, Salmo salar L., management is that river flow influences their upstream migration; but the quantitative relationships between flow and movements are variable and inconsistent. A consensus has emerged that standard rules on salmon flow needs for water management across all rivers are unattainable. However, this does not preclude an underlying conceptual framework that should guide a consistent scientific basis to flow management for protecting salmon. This article examines the potential for a conceptual framework from a British Isles perspective, assuming that upstream migration is an emergent property from selection to optimise lifetime fitness. The template for this adaptation is the diversity of river types and hydro‐morphology in British rivers coupled with life‐history and migration adaptations that may be influenced by flow‐related factors. Models of adult salmon migration through estuaries and rivers are outlined that may provide a basis for developing generic guidance.

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.

Are Females Maternal Manipulators, Selfish Mothers, Or Both? Insight from Pythons

Abstract During reproduction, females often modify their behavior relative to the nonreproductive condition. These changes are frequently attributed to maternal efforts to optimize offspring development and survival (i.e., the maternal manipulation hypothesis). However, Schwarzkopf and Andrews (2012) recently challenged this concept as oversimplified, emphasizing that females should optimize their own lifetime fitness, and therefore maternal efforts may be directed at the female's future reproductive effort in addition, or even in contrast, to current reproductive effort. To provide insight into the relative importance of current versus future reproductive effort in shaping maternal behavior, we systematically explore a single study system—pythons. Pythons show distinct maternal behaviors during gravidity (modified basking effort), peri-oviposition (nest site selection), and postoviposition (egg brooding). By examining each component, we reveal that python maternal effort is predominantly aimed at current...

Caterpillars use developmental plasticity and diet choice to overcome the early life experience of nutritional imbalance

Nutritional conditions experienced during early growth have important implications for the lifetime fitness of herbivores in nutritionally heterogeneous environments. We investigated the early life effects of imbalanced nutrient intake on key fitness components and how such effects can be overcome in a generalist leaf-feeding lepidopteran caterpillar, Spodoptera litura. Over the fifth larval instar, caterpillars were pretreated on one of three diets that varied in protein and carbohydrate content (p35:c7, p21:c21 or p7:c35; % dry mass). After moulting to the sixth instar, they were transferred to one of three no-choice diets (p35:c7, p21:c21 or p7:c35) or a food choice where they received two nutritionally complementary diets (p35:c7 versus p7:c35). Approximately 80% of caterpillars that had been protein-deprived (p7:c35) during the fifth instar moulted to the seventh instar and developed into heavier pupae than those pupating after the sixth instar. The threshold body mass for pupal metamorphosis was 144 mg at the start of the sixth instar. Ingesting a diet low in protein or carbohydrate during the early instar led to a deficit in body protein or lipid content, respectively. When given a choice, caterpillars pretreated on the low-protein diet (p7:c35) selected significantly more protein and thus had a higher intake ratio of protein to carbohydrate than those from other diets (p35:c7, p21:c21). Our results suggest that caterpillars are not only capable of switching their developmental program to reduce the deleterious effects of an early deficiency of protein, but also flexible at adjusting nutrient preferences to redress specific nutritional imbalances experienced early in life.

Sperm as a limiting factor in mating success in Hymenoptera parasitoids

AbstractThe paradigm that females produce few costly eggs, whereas males produce an unlimited quantity of sperm holds true when matings are dispersed over time and males can replenish their sperm supply. In such a system, the best strategy for males is to mate with as many females as possible, as more is always better. However, in parasitoid species, mating often occurs at the emergence site and males may have to mate successively several females in a short period of time. This can lead to sperm depletion that can be temporary in synspermatogenic species whose males produce sperm throughout their adult life, or definitive in prospermatogenic species whose males emerge with their full sperm complement and do not produce more during their adult life. Both the spermatogeny index and the mating structure of a species will therefore influence the probability and intensity of sperm depletion in males. Sperm‐limited males can court and mate females even in prospermatogenic species. These males still gain some inclusive fitness by preventing competitor males to fully inseminate females, therefore increasing the representation of their daughters in the following generation. Females that mate with partially or completely sperm‐depleted males produce a constrained sex ratio that decreases their lifetime fitness. In species where sperm‐depleted males occur, female choosiness based on sperm supply is predicted, as the cost of mating sperm‐depleted males can be high. In addition, males are also expected to be choosy in prospermatogenic species as mating with sub‐optimal females can be costly when sperm is limited.

Role of climate and competitors in limiting fitness across range edges of an annual plant

It is often assumed that the geographic distributions of species match their climatic tolerances, but this assumption is not frequently tested. Moreover, few studies examine the relative importance of abiotic and biotic factors for limiting species ranges. We combined multiple approaches to assess the extent to which fitness of a widespread native annual legume, Chamaecrista fasciculata, decreases at and beyond its northern and western range edges, and how this is influenced by the presence of neighbors. First, we examined plant fitness and the effect of neighbors in natural populations at different geographic range locations for three years. Fitness decreased toward the northern range edge, but not the western edge. Neighbor removal had a consistently positive effect on seedpod production across all years and sites. Second, we established experimental populations at sites within the range, and at and beyond the northern and western range edges. We tracked individual fitness and recorded seedling recruitment in the following year (a complete generation) to estimate population growth rate. Individual fitness and population growth declined to near zero beyond both range edges, indicating that C. fasciculata with its present genetic composition will not establish in these regions, given conditions currently. We also carried out a neighbor removal treatment. Consistent with the natural populations, neighbors reduced seedpod production of reproductive adults. However, neighbors also increased early-season survival, and this positive effect early in life history resulted in a net positive effect of neighbors on lifetime fitness at most range locations. Our data show that the population growth rate of C. fasciculata includes values above replacement, and populations are well adapted to conditions up to the edge of the range, whereas the severely compromised fitness at sites beyond the edge precludes immediate establishment of populations and thereby impedes adaptation to these conditions.

Bad coat, ripped genes: cryptic selection on coat colour varies with ontogeny in Soay sheep

A fundamental goal for evolutionary biologists is to connect the processes of natural selection and genetic drift with the maintenance of genetic variation in the wild. There are now scores of examples in which mapping phenotypes to genotypes has identified the molecular basis of traits in natural populations, but documenting the fitness consequences of these genes has proven more elusive. A long-term study of several thousand unmanaged sheep on the remote Scottish island of Hirta in the St. Kilda archipelago provides a unique opportunity to make these connections between genotype, phenotype and fitness. Since 1985, there has been a steady decline in the frequency of sheep with a rare uniform ('self'-) pigmentation pattern as opposed to the more common wild-type pattern of dark upper body and pale belly. In this issue of Molecular Ecology, Gratten et al. (2012) link variation at the agouti signalling protein (ASIP) gene with 25 years of pedigree information and individual fitness data to investigate the contributions of natural selection and genetic drift to this decline. Consistent with the decrease in frequency of self-type sheep, Gratten et al. demonstrate that recessive genetic variants at ASIP are associated with reduced lifetime fitness. But surprisingly, these variants show the opposite trend to the self-type phenotype by increasing throughout the study period. This paradoxical result occurs because heterozygotes that harbour the majority of self-type alleles have increased in frequency. This pattern would not have been detectable if only phenotype had been monitored because the pigmentation pattern of heterozygotes is indistinguishable from that of wild-type homozygotes. The study provides an excellent example of the importance of measuring selection at both the phenotypic and genetic level, and demonstrates how long-term pedigrees can be used to link alleles to phenotypes and ultimately to fitness.

Complex consequences of herbivory and interplant cues in three annual plants.

Information exchange (or signaling) between plants following herbivore damage has recently been shown to affect plant responses to herbivory in relatively simple natural systems. In a large, manipulative field study using three annual plant species (Achyrachaena mollis, Lupinus nanus, and Sinapis arvensis), we tested whether experimental damage to a neighboring conspecific affected a plant's lifetime fitness and interactions with herbivores. By manipulating relatedness between plants, we assessed whether genetic relatedness of neighboring individuals influenced the outcome of having a damaged neighbor. Additionally, in laboratory feeding assays, we assessed whether damage to a neighboring plant specifically affected palatability to a generalist herbivore and, for S. arvensis, a specialist herbivore. Our study suggested a high level of contingency in the outcomes of plant signaling. For example, in the field, damaging a neighbor resulted in greater herbivory to A. mollis, but only when the damaged neighbor was a close relative. Similarly, in laboratory trials, the palatability of S. arvensis to a generalist herbivore increased after the plant was exposed to a damaged neighbor, while palatability to a specialist herbivore decreased. Across all species, damage to a neighbor resulted in decreased lifetime fitness, but only if neighbors were closely related. These results suggest that the outcomes of plant signaling within multi-species neighborhoods may be far more context-specific than has been previously shown. In particular, our study shows that herbivore interactions and signaling between plants are contingent on the genetic relationship between neighboring plants. Many factors affect the outcomes of plant signaling, and studies that clarify these factors will be necessary in order to assess the role of plant information exchange about herbivory in natural systems.

Frequent skipped spawning in the world’s largest cod population

Life-history theory suggests that animals may skip reproductive events after initial maturation to maximize lifetime fitness. In iteroparous teleosts, verifying past spawning history is particularly difficult; the degree of skipped spawning at the population level therefore remains unknown. We unequivocally show frequent skipped spawning in Northeast Arctic cod (NEAC) in a massive field and laboratory effort from 2006 to 2008. This was verified by postovulatory follicles in temporarily arrested ovaries close to the putative spawning period. At the population level, "skippers" were estimated to be approximately equally abundant as spawning females in 2008, constituting ∼24% of the females 60-100 cm. These females never truly started vitellogenesis and principally remained on the feeding grounds when spawners migrated southward, avoiding any migration costs. The proximate cause of skipping seems to be insufficient energy to initiate oocyte development, indicating that skipped spawning may partly be a density-dependent response important in population regulation. Our data also indicate more skipping among smaller females and potential tradeoffs between current and future reproductive effort. We propose that skipped spawning is an integral life-history component for NEAC, likely varying annually, and it could therefore be an underlying factor causing some of the currently unexplained large NEAC recruitment variation. The same may hold for other teleosts.

Interactions between soil habitat and geographic range location affect plant fitness.

Populations are often found on different habitats at different geographic locations. This habitat shift may be due to biased dispersal, physiological tolerances or biotic interactions. To explore how fitness of the native plant Chamaecrista fasciculata depends on habitat within, at and beyond its range edge, we planted seeds from five populations in two soil substrates at these geographic locations. We found that with reduced competition, lifetime fitness was always greater or equivalent in one habitat type, loam soils, though early-season survival was greater on sand soils. At the range edge, natural populations are typically found on sand soil habitats, which are also less competitive environments. Early-season survival and fitness differed among source populations, and when transplanted beyond the range edge, range edge populations had greater fitness than interior populations. Our results indicate that even when the optimal soil substrate for a species does not change with geographic range location, the realized niche of a species may be restricted to sub-optimal habitats at the range edge because of the combined effects of differences in abiotic and biotic effects (e.g. competitors) between substrates.

Nondestructive sampling of insect DNA from defensive secretion

Nondestructive techniques to obtain DNA from organisms can further genetic analyses such as estimating genetic diversity, dispersal and lifetime fitness, without permanently removing individuals from the population or removing body parts. Possible DNA sources for insects include frass, exuviae, and wing and leg clippings. However, these are not feasible approaches for organisms that cannot be removed from their natural environment for long periods or when adverse effects of tissue removal must be avoided. This study evaluated the impacts and efficacy of extracting haemolymph from a defensive secretion to obtain DNA for amplification of microsatellites using a nondestructive technique. A secretion containing haemolymph was obtained from Bolitotherus cornutus (the forked fungus beetle) by perturbation of the defensive gland with a capillary tube. A laboratory experiment demonstrated that the sampling methodology had no impact on mortality, reproductive success or gland expression. To evaluate the quality of DNA obtained in natural samples, haemolymph was collected from 187 individuals in the field and successfully genotyped at nine microsatellite loci for 95.7% of samples. These results indicate that haemolymph-rich defensive secretions contain DNA and can be sampled without negative impacts on the health or fitness of individual insects.

Parental care trade-offs and the role of filial cannibalism in the maritime earwig, Anisolabis maritima

Animals that provide parental care are expected to weigh the value of current offspring against the value of future offspring, such that total investment across all offspring is allocated to maximize lifetime fitness. In this study, we characterize the trade-offs associated with maternal care in the maritime earwig, Anisolabis maritima (Dermaptera: Anisolabididae). We measured the benefits of care in terms of hatching success through removal experiments and the costs of care by comparing the future fecundity of caring females to that of removals. We show that the benefits of care greatly outweigh the costs, providing a seven-fold increase in hatching success. Artificially removed females had larger subsequent clutches and shorter internest intervals, but very low hatching success. Naturally abandoning females always cannibalize all their eggs. Partial clutch cannibalism was a ubiquitous feature of maternal care, although rates were variable among individuals. In post hoc tests, we first addressed the ultimate explanation that filial cannibalism is a way for females to facultatively adjust their investment per clutch in order to maximize future reproduction. We then tested two proximate explanations for filial cannibalism: (1) females that lay more eggs for their given body size tend to consume more eggs, reflecting a nutritional deficiency; (2) females prefer to cannibalize the youngest eggs to reduce the overall duration of egg care. In addition, we consider the alternative explanation that females eat unviable eggs for hygienic reasons. Our results provide support for both energy limitation and hygienic maintenance. Higher rates of egg cannibalism near the very end of nesting were also suggestive of nymphal cannibalism, a phenomenon that will be examined in future work.

Selection and microevolution of coat pattern are cryptic in a wild population of sheep

Understanding the maintenance of genetic variation in natural populations is a core aim of evolutionary genetics. Insight can be gained by quantifying selection at the level of the genotype, as opposed to the phenotype. Here, we show that in a natural population of Soay sheep which is polymorphic for coat pattern, recessive genetic variants at the causal gene, agouti signalling protein (ASIP) are associated with reduced lifetime fitness. This was due primarily to a reduction in juvenile survival of uniformly coloured (self-type) sheep, which are homozygous recessive, and occurs despite significantly higher reproductive success in surviving self-type adults. Consistent with their relatively low fitness, we show that the frequency of self-type individuals has declined from 1985 to 2008. Remarkably though, the frequency of the underlying self-allele has increased, because the frequency of heterozygous individuals (who harbour the majority of all self-alleles) has increased. Indeed, the ratio of observed/expected heterozygous individuals has increased during the study, such that there is now a significant excess of heterozygotyes. By employing gene-dropping simulations, we show that microevolutionary trends in the frequency and excess of ASIP heterozygotes are too pronounced to be caused by genetic drift. Studying this polymorphism at the level of phenotype rather than underlying genotype would have failed to detect cryptic fitness differences. We would also have been unable to rule out genetic drift as an evolutionary force driving genetic change. This highlights the importance of resolving the underlying genetic basis of phenotypic variation in explaining evolutionary dynamics.