Artificial selection,pre‐release diet,and gut symbiont inoculation effects on sterile male longevity for area‐wide fruit‐fly management

Longevity is an important life‐history trait for successful and cost‐effective application of the sterile insect technique. Furthermore, it has been shown that females of some species – e.g., Anastrepha ludens (Loew) (Diptera: Tephritidae) – preferentially copulate with ‘old’, sexually experienced males, rather than younger and inexperienced males. Long‐lived sterile males may therefore have greater opportunity to find and mate with wild females than short‐lived males, and be more effective in inducing sterility into wild populations. We explored the feasibility of increasing sterile male lifespan through selection of long‐lived strains and provision of pre‐release diets with added protein, and inoculated with bacterial symbionts recovered from cultures of the gut of wild Anastrepha obliqua (Macquart). Artificial selection for long‐lived A. ludens resulted in a sharp drop of fecundity levels for F1 females. Nevertheless, the cross of long‐lived males with laboratory females produced a female F1 progeny with fecundity levels comparable to those of females in the established colony. However, the male progeny of long‐lived males*laboratory females did not survive in higher proportions than laboratory males. Provision of sugar to A. obliqua adults resulted in increased survival in comparison to adults provided only with water, whereas the addition of protein to sugar‐only diets had no additional effect on longevity. Non‐irradiated males lived longer than irradiated males, and supplying a generic probiotic diet produced no noticeable effect in restoring irradiated male longevity of A. obliqua. We discuss the need to evaluate the time to reach sexual maturity and survival under stress for long‐lived strains, and the inclusion of low amounts of protein and specific beneficial bacteria in pre‐release diets to increase sterile male performance and longevity in the field.     

Heterosis in age‐specific selected populations of a seed beetle: Sex differences in longevity and reproductive behavior

We tested mutation accumulation hypothesis for the evolution of senescence using short‐lived and long‐lived populations of the seed‐feeding beetle, Acanthoscelides obtectus (Say), obtained by selection on early‐ and late‐life for many generations. The expected consequence of the mutation accumulation hypothesis is that in short‐lived populations, where the force of natural selection is the strongest early in life, the late‐life fitness traits should decline due to genetic drift which increases the frequency of mutations with deleterious effects in later adult stages. Since it is unlikely that identical deleterious mutations will increase in several independent populations, hybrid vigor for late‐life fitness is expected in offspring obtained in crosses among populations selected for early‐life fitness traits. We tested longevity of both sexes, female fecundity and male reproductive behavior for hybrid vigor by comparing hybrid and nonhybrid short‐lived populations. Hybrid vigor was confirmed for male virility, mating speed and copulation duration, and longevity of both sexes at late ages. In contrast to males, the results on female fecundity in short‐lived populations did not support mutation accumulation as a genetic mechanism for the evolution of this trait. Contrary to the prediction of this hypothesis, male mating ability indices and female fecundity in long‐lived populations exhibited hybrid vigor at all assayed age classes. We demonstrate that nonhybrid long‐lived populations diverged randomly regarding female and male reproductive fitness, indicating that sexually antagonistic selection, when accompanied with genetic drift for female fecundity and male virility, might be responsible for overriding natural selection in the independently evolving long‐lived populations.     

Effect of habitat area and isolation on plant trait distribution in European forests and grasslands

A number of studies show contrasting results in how plant species with specific life‐history strategies respond to fragmentation, but a general analysis on whether traits affect plant species occurrences in relation to habitat area and isolation has not been performed. We used published data from forests and grasslands in north‐central Europe to analyse if there are general patterns of sensitivity to isolation and dependency of area for species using three traits: life‐span, clonality, and seed weight. We show that a larger share of all forest species was affected by habitat isolation and area as compared to grassland species. Persistence‐related traits, life‐span and clonality, were associated to habitat area and the dispersal and recruitment related trait, seed weight, to isolation in both forest and grassland patches. Occurrence of clonal plant species decreased with habitat area, opposite to non‐clonal plant species, and long‐lived plant species decreased with grassland area. The directions of these responses partly challenge some earlier views, suggesting that further decrease in habitat area will lead to a change in plant species community composition, towards relatively fewer clonal and long‐lived plants with large seeds in small forest patches and fewer clonal plants with small seeds in small grassland patches. It is likely that this altered community has been reached in many fragmented European landscapes consisting of small and isolated natural and semi‐natural patches, where many non‐clonal and short‐lived species have already disappeared. Our study based on a large‐scale dataset reveals general and useful insights concerning area and isolation effects on plant species composition that can improve the outcome of conservation and restoration efforts of plant communities in rural landscapes.     

Has gene duplication impacted the evolution of Eutherian longevity?

One of the greatest unresolved questions in aging biology is determining the genetic basis of interspecies longevity variation. Gene duplication is often the key to understanding the origin and evolution of important Eutherian phenotypes. We systematically identified longevity‐associated genes in model organisms that duplicated throughout Eutherian evolution. Longevity‐associated gene families have a marginally significantly higher rate of duplication compared to non‐longevity‐associated gene families. Anti‐longevity‐associated gene families have significantly increased rate of duplication compared to pro‐longevity gene families and are enriched in neurodegenerative disease categories. Conversely, duplicated pro‐longevity‐associated gene families are enriched in cell cycle genes. There is a cluster of longevity‐associated gene families that expanded solely in long‐lived species that is significantly enriched in pathways relating to 3‐UTR‐mediated translational regulation, metabolism of proteins and gene expression, pathways that have the potential to affect longevity. The identification of a gene cluster that duplicated solely in long‐lived species involved in such fundamental processes provides a promising avenue for further exploration of Eutherian longevity evolution.     

Proteomics of Long‐Lived Mammals

Mammalian species differ up to 100‐fold in their aging rates and maximum lifespans. Long‐lived mammals appear to possess traits that extend lifespan and healthspan. Genomic analyses have not revealed a single pro‐longevity function that would account for all longevity effects. In contrast, it appears that pro‐longevity mechanisms may be complex traits afforded by connections between metabolism and protein functions that are impossible to predict by genomic approaches alone. Thus, metabolomics and proteomics studies will be required to understand the mechanisms of longevity. Several examples are reviewed that demonstrate the naked mole rat (NMR) shows unique proteomic signatures that contribute to longevity by overcoming several hallmarks of aging. SIRT6 is also discussed as an example of a protein that evolves enhanced enzymatic function in long‐lived species. Finally, it is shown that several longevity‐related proteins such as Cip1/p21, FOXO3, TOP2A, AKT1, RICTOR, INSR, and SIRT6 harbor posttranslational modification (PTM) sites that preferentially appear in either short‐ or long‐lived species and provide examples of crosstalk between PTM sites. Prospects of enhancing lifespan and healthspan of humans by altering metabolism and proteoforms with drugs that mimic changes observed in long‐lived species are discussed.     

Differential response to larval crowding of a long‐ and a short‐lived medfly biotype

Response of endophytic fruit fly species (Tephritidae) to larval crowding is a form of scramble competition that may affect important life history traits of adults, such as survival and reproduction. Recent empirical evidence demonstrates large differences in adult life history traits, especially longevity, among Mediterranean fruit fly (Ceratitis capitata; "medfly") biotypes obtained from different regions of the world. However, whether the evolution of long lifespan is associated with response to stress induced by larval crowding has not been fully elucidated. We investigated, under constant laboratory conditions, the response of a short‐ and a long‐lived medfly biotypes to stress induced by larval crowding. Survival and development of larvae and pupae and the size of resulting pupae were recorded. The lifespan and age‐specific egg production patterns of the obtained adults were recorded. Our findings reveal that increased larval density reduced immature survival (larvae and pupae) in the short‐lived biotype but had rather neutral effects on the longed‐lived one. Only larvae of the long‐lived biotype were capable of prolonging their developmental duration under the highest crowding regime to successfully pupate and emerge as adults. Response of emerging adults to larvae crowding conditions was similar in the two medfly biotypes. Those individuals emerging from high larval density regimes had reduced longevity and fecundity. Long‐lived biotype individuals, however, appeared to suffer a higher cost in longevity compared with the short‐lived one. The importance of our findings to understand the evolution of long lifespan is discussed.     

Both biotic and abiotic factors influence floral longevity in three species of Epidendrum (Orchidaceae)

Extended flower longevity has been widely defended to occur as a consequence of low pollination activity. To test this hypothesis in Neotropical rainforests, we selected three species of Epidendrum that flower during rainy conditions and commonly exhibit low levels of insect visits. Experimental studies carried out in 15 populations distributed along a wide spatial gradient detected the presence of pollinator limitation in all populations. Pollinia removal without pollen deposition increased longevity, and thus extended longevity could apparently be considered as an ecological advantage for these orchids. Nevertheless, flower longevity was severely shortened by abiotic factors like precipitation and humidity. Comparison with other tropical orchids showed that flower longevity was higher even in species that flower during periods of more pollinator activity than the ones studied here, which is contrary to the hypothesis that pollinators are the only driving force for long‐lived flowers in Epidendrum. Thus, although long floral longevities are apparently favorable for the reproductive success of these species, the high maintenance costs experienced during rainy conditions are also an important factor constraining the selection of long‐lived flowers in Epidendrum.     

Effects of diet restriction on life history in a sexually cannibalistic spider

Diet restriction increases longevity while reducing fecundity in a broad range of organisms. However, there are exceptions to this rule, and the causes of these exceptions remain unclear. One hypothesis is that short‐lived, semelparous organisms gain no benefit from increased longevity regardless of nutritional resources. Another hypothesis is that organisms may alter their behaviour to compensate for nutrient deficiencies. We examined these hypotheses in the colonial orb‐weaving spider Cyrtophora citricola. Sexual cannibalism is frequent in this species so that females are long lived and interoparous while males are semelparous. Because of these differing sexual strategies, we predicted that the common pattern of increased longevity under diet restriction would hold for females but not for males. We also investigated in a semi‐natural setting whether spiders could compensate for diet restriction by altering their feeding behaviour. Diet‐restricted females produced fewer offspring but lived longer than well‐fed females, while diet had no effect on male longevity. Despite being semelparous, virgin males were quite long‐lived, suggesting that potential lifespan is relatively unimportant in determining the effects of diet restriction. Contrary to our predictions, females were unable to compensate for their restricted diet by altering their foraging behaviour. Instead, semi‐natural conditions increased the differences between spiders on high and low diets, suggesting that the effects of diet restriction can be pervasive under natural conditions.     

Exome sequencing of three cases of familial exceptional longevity

Exceptional longevity (EL) is a rare phenotype that can cluster in families, and co‐segregation of genetic variation in these families may point to candidate genes that could contribute to extended lifespan. In this study, for the first time, we have sequenced a total of seven exomes from exceptionally long‐lived siblings (probands ≥ 103 years and at least one sibling ≥ 97 years) that come from three separate families. We have focused on rare functional variants (RFVs) which have ≤ 1% minor allele frequency according to databases and that are likely to alter gene product function. Based on this, we have identified one candidate longevity gene carrying RFVs in all three families, APOB. Interestingly, APOB is a component of lipoprotein particles together with APOE, and variants in the genes encoding these two proteins have been previously associated with human longevity. Analysis of nonfamilial EL cases showed a trend, without reaching statistical significance, toward enrichment of APOB RFVs. We have also identified candidate longevity genes shared between two families (5–13) or within individual families (66–156 genes). Some of these genes have been previously linked to longevity in model organisms, such as PPARGC1A, NRG1, RAD52, RAD51, NCOR1, and ADCY5 genes. This work provides an initial catalog of genes that could contribute to exceptional familial longevity.     

Family Affects Sibling Cannibalism in the Black Widow Spider,Latrodectus hesperus

Adaptive foraging tactics are shaped by genes, the environment and gene–environment interactions. Because of relatively high levels of agonism toward conspecifics, spiders have been a popular focus for behavioral–ecological examinations of conspecific predation, or cannibalism. Surprisingly, studies examining the underlying, proximate assumption that cannibalism in spiders is a heritable trait shaped by interactions between genes and the environment are virtually non‐existent. Here, we examine the influence of family on the expression of sibling cannibalism in the post‐hatching, group‐living phase of an otherwise solitary, web‐building spider, the North American black widow (Latrodectus hesperus). Our results showed significant levels of variation in cannibalistic propensity among 26 sibships, with some families cannibalizing full sibs within 2 d and other families waiting 3 wk before resorting to cannibalism. A similar family‐level effect was evident in measures of sibling cohabitation, voracity toward cricket prey, and development speed. Negative correlations between maternal egg sac investment and offspring cannibalism suggest that this family effect may stem, at least in part, from a maternal effect, although we were not able to directly test the prediction that cannibalism is most common from spiderlings in poor condition. Thus, we present novel data suggesting family effects seem to be responsible for cannibalism in L. hesperus spiderlings; however, future work will be required to disentangle the relative importance of shared genes and shared maternal environment. We discuss several mechanisms that could explain the persistence of family‐level variation in cannibalism, a trait that seems likely to be subject to strong directional selection.     

Differences in boldness are repeatable and heritable in a long‐lived marine predator

Animal personalities, composed of axes of consistent individual behaviors, are widely reported and can have important fitness consequences. However, despite theoretical predictions that life‐history trade‐offs may cause and maintain personality differences, our understanding of the evolutionary ecology of personality remains poor, especially in long‐lived species where trade‐offs and senescence have been shown to be stronger. Furthermore, although much theoretical and empirical work assumes selection shapes variation in personalities, studies exploring the genetic underpinnings of personality traits are rare. Here we study one standard axis of personality, the shy–bold continuum, in a long‐lived marine species, the wandering albatross from Possession Island, Crozet, by measuring the behavioral response to a human approach. Using generalized linear mixed models in a Bayesian framework, we show that boldness is highly repeatable and heritable. We also find strong differences in boldness between breeding colonies, which vary in size and density, suggesting birds are shyer in more dense colonies. These results demonstrate that in this seabird population, boldness is both heritable and repeatable and highlights the potential for ecological and evolutionary processes to shape personality traits in species with varying life‐history strategies.     

Rate of resistance evolution and polymorphism in long‐ and short‐lived hosts

Recent theoretical work has shown that long‐lived hosts are expected to evolve higher equilibrium levels of disease resistance than shorter‐lived hosts, but questions of how longevity affects the rate of resistance evolution and the maintenance of polymorphism remain unanswered. Conventional wisdom suggests that adaptive evolution should occur more slowly in long‐lived organisms than in short‐lived organisms. However, the opposite may be true for the evolution of disease‐resistance traits where exposure to disease, and therefore the strength of selection for resistance increases with longevity. In a single locus model of innate resistance to a frequency‐dependent, sterilizing disease, longer lived hosts evolved resistance more rapidly than short‐lived hosts. Moreover, resistance in long‐lived hosts could only be polymorphic for more costly and more extreme resistance levels than short‐lived hosts. The increased rate of evolution occurred in spite of longer generation times because longer‐lived hosts had both a longer period of exposure to disease as well as higher disease prevalence. Qualitatively similar results were found when the model was extended to mortality‐inducing diseases, or to density‐dependent transmission modes. Our study shows that the evolutionary dynamics of host resistance is determined by more than just levels of resistance and cost, but is highly sensitive to the life‐history traits of the host.     

The growth hormone receptor gene‐disrupted mouse fails to respond to an intermittent fasting diet

The interaction of longevity‐conferring genes with longevity‐conferring diets is poorly understood. The growth hormone receptor gene‐disrupted (GHR‐KO) mouse is long lived; and this longevity is not responsive to 30% caloric restriction, in contrast to wild‐type animals from the same strain. To determine whether this may have been limited to a particular level of dietary restriction, we subjected GHR‐KO mice to a different dietary restriction regimen, an intermittent fasting diet. The intermittent fasting diet increased the survivorship and improved insulin sensitivity of normal males, but failed to affect either parameter in GHR‐KO mice. From the results of two paradigms of dietary restriction, we postulate that GHR‐KO mice would be resistant to any manner of dietary restriction; potentially due to their inability to further enhance insulin sensitivity. Insulin sensitivity may be a mechanism and/or a marker of the lifespan extending potential of an intervention.     

Persistence,multiple demographic strategies and conservation in long‐lived Mediterranean plants

Abstract. Persistence by longevity has been rarely considered as an alternative to regeneration by seeding for plants showing multiple demographic strategies. We propose a conceptual model of multiple demographic strategies for long‐lived plants in stable habitats, shifting from regeneration by seeding to persistence by longevity and/or vegetative reproduction, along gradients of abiotic stress or interspecific competition. Regeneration by seeding would be promoted under low abiotic stress or under low competition, whereas persistence by longevity and/or vegetative reproduction would predominate at high levels of abiotic stress or competition. We test this model with two threatened species of the Mediterranean region, the shrub Juniperus communis, a widely distributed species which maintains relict populations in the Mediterranean mountains thanks to great adult longevity and Pinguicula vallisneriifolia, a palaeo‐endemic herb relying on a perennial habit and vegetative reproduction under drought imposed stress or high competition at late successional phases. As a main consequence, multiple demographic strategies enhance a plant's ability to exploit environmental heterogeneity at different spatial (patches, localities, regions within the species’ distribution area) and temporal (individual life span, glacial‐interglacial cycles) scales. The potential of multiple demographic dynamics based on persistence and regeneration must be considered as a major ecological trait determining the long‐term viability of peripheral populations of relict species as well as the inertia against extinction of many threatened endemisms, thereby contributing to the maintenance of the high plant diversity characterizing the Mediterranean region.     

Is N‐resorption efficiency related to secondary compounds and leaf longevity in coexisting plant species of the arid Patagonian Monte,Argentina?

Leaf longevity and nutrient resorption efficiency are important strategies to conserve plant nutrients. Theory suggests a negative relationship between them and also proposes that high concentration of phenolics in long‐lived leaves may reduce nutrient resorption. In order to provide new evidence on these relationships, we explored whether N‐resorption efficiency is related to leaf longevity, secondary compounds and other leaf traits in coexisting plant species of different life forms in the arid Patagonian Monte, Argentina. We assessed N‐resorption efficiency, green leaf traits (leaf mass per area (LMA), leaf longevity and lignin, total soluble phenolics and N concentrations) and N concentration in senescent leaves of 12 species of different life forms (evergreen shrubs, deciduous shrubs and perennial grasses) with contrasting leaf traits. We found that leaf longevity was positively correlated to LMA and lignin, and negatively correlated to N concentration in green leaves. N concentrations both in green and senescent leaves were positively related. N‐resorption efficiency was not associated with the concentration of secondary compounds (total soluble phenolics and lignin) but it was negatively related to LMA and leaf longevity and positively related to N concentration in green leaves. Furthermore, leaf traits overlapped among life forms highlighting that life forms are not a good indicator of the functional properties (at least in relation to nutrient conservation) of species. In conclusion, our findings indicated that differences in N‐resorption efficiency among coexisting species were more related to N concentration in green leaves, leaf lifespan and LMA than to the presence of secondary compounds at least those assessed in our study (soluble phenolics and lignin). Accordingly, N‐resorption efficiency seems to be modulated, at least in part, by the productivity–persistence trade‐off.     

Experience versus effort: what explains dynamic heterogeneity with respect to age?

Age‐related patterns of survival and reproduction have been explained by accumulated experience (‘experience hypothesis’), increased effort (‘effort hypothesis’), and intrinsic differences in phenotypes (‘selection hypothesis’). We examined the experience and effort hypotheses using a 40‐year data set in a population of Leach's storm‐petrels Oceanodroma leucorhoa, long‐lived seabirds for which the effect of phenotypic variation has been previously demonstrated. Age was quantified by time since recruitment (‘breeding age’). The best model of adult survival included a positive effect of breeding age (1, 2, 3+ years), sex (male > female), and year. Among‐individuals variation (fixed heterogeneity) accounted for 31.6% of the variance in annual reproductive success. We further examined within‐individual patterns in reproductive success (dynamic heterogeneity) in the subset of individuals with at least five breeding attempts. Three distinct phases characterized reproductive success – early increase, long asymptotic peak, late decline. No effect of early reproductive output on longevity was found, however, early success was positively correlated with lifetime reproductive success. Reproductive success was lower earlier than later in life. Among the few natally philopatric individuals in the population, age of first breeding had no effect on longevity, lifetime reproductive success, or early reproductive success. No support for the effort hypothesis was found in this population. Instead, age‐specific patterns of survival and reproduction in these birds are best explained by the experience hypothesis over and above the effect of intrinsic differences among individuals.     

Stressful environments can indirectly select for increased longevity

Longevity is modulated by a range of conserved genes in eukaryotes, but it is unclear how variation in these genes contributes to the evolution of longevity in nature. Mutations that increase life span in model organisms typically induce trade‐offs which lead to a net reduction in fitness, suggesting that such mutations are unlikely to become established in natural populations. However, the fitness consequences of manipulating longevity have rarely been assessed in heterogeneous environments, in which stressful conditions are encountered. Using laboratory selection experiments, we demonstrate that long‐lived, stress‐resistant Caenorhabditis elegans age‐1(hx546) mutants have higher fitness than the wild‐type genotype if mixed genotype populations are periodically exposed to high temperatures when food is not limited. We further establish, using stochastic population projection models, that the age‐1(hx546) mutant allele can confer a selective advantage if temperature stress is encountered when food availability also varies over time. Our results indicate that heterogeneity in environmental stress may lead to altered allele frequencies over ecological timescales and indirectly drive the evolution of longevity. This has important implications for understanding the evolution of life‐history strategies.     

Genetic variation in variability: Phenotypic variability of fledging weight and its evolution in a songbird population

Variation in traits is essential for natural selection to operate and genetic and environmental effects can contribute to this phenotypic variation. From domesticated populations, we know that families can differ in their level of within‐family variance, which leads to the intriguing situation that within‐family variance can be heritable. For offspring traits, such as birth weight, this implies that within‐family variance in traits can vary among families and can thus be shaped by natural selection. Empirical evidence for this in wild populations is however lacking. We investigated whether within‐family variance in fledging weight is heritable in a wild great tit (Parus major) population and whether these differences are associated with fitness. We found significant evidence for genetic variance in within‐family variance. The genetic coefficient of variation (GCV) was 0.18 and 0.25, when considering fledging weight a parental or offspring trait, respectively. We found a significant quadratic relationship between within‐family variance and fitness: families with low or high within‐family variance had lower fitness than families with intermediate within‐family variance. Our results show that within‐family variance can respond to selection and provides evidence for stabilizing selection on within‐family variance.