The evolution of life histories in spatially heterogeneous environments: Optimal reaction norms revisited

Summary Natural populations live in heterogeneous environments, where habitat variation drives the evolution of phenotypic plasticity. The key feature of population structure addressed in this paper is the net flow of individuals from source (good) to sink (poor) habitats. These movements make it necessary to calculate fitness across the full range of habitats encountered by the population, rather than independently for each habitat. As a consequence, the optimal phenotype in a given habitat not only depends on conditions there but is linked to the performance of individuals in other habitats. We generalize the Euler-Lotka equation to define fitness in a spatially heterogeneous environment in which individuals disperse among habitats as newborn and then stay in a given habitat for life. In this case, maximizing fitness (the rate of increase over all habitats) is equivalent to maximizing the reproductive value of newborn in each habitat but not to maximizing the rate of increase that would result if individuals in each habitat were an isolated population. The new equation can be used to find optimal reaction norms for life history traits, and examples are calculated for age at maturity and clutch size. In contrast to previous results, the optimal reaction norm differs from the line connecting local adaptations of isolated populations each living in only one habitat. Selection pressure is higher in good and frequent habitats than in poor and rare ones. A formula for the relative importance of these two factors allows predictions of the habitat in which the genetic variance about the optimal reaction norm should be smallest.     

Breeding site characteristics regulating life history traits of the brown tree frog, Litoria ewingii

Past research has determined the habitat requirements of amphibian species predominantly from presence/absence studies. This study tested the hypothesis that relationships between breeding site habitat components, life history traits and fitness may provide a higher resolution of biological data relating to the habitat requirements of amphibian species. We tested this novel approach by using Litoria ewingii as our model species. We correlated larval and metamorph life history traits with habitat variables at 28 small to medium sized ponds within a commercially logged forest in southern Tasmania, Australia. To avoid larval mortality due to pond desiccation, L. ewingii laid eggs and metamorphosed earlier in smaller ponds. Snout vent length at metamorphosis increased with elevation and metamorphosis was earlier in less shaded ponds. Breeding ponds that maximised the fitness of L. ewingii were higher elevation ponds with reduced shading, steeper bank slopes and reduced pond isolation. The findings of the study equip land managers with a greater ecological understanding of ecosystem function in relation to specific species. The methodological approach has broad application to conservation biology where an awareness of the specific habitat requirements of amphibians is critical to successful ecosystem management.     

The fitness functions associated with diapause induction in arthropods I. The effects of age structure

This paper analyzes the effects of age structure on the shape of the fitness functions associated with diapause induction in arthropods and presents the following results: (1) The shape of the fitness function depends on three variables: age structure (specifically the time course of individuals passing through the end of the sensitive period), the position of the optimal time to switch to diapause, and the end of the season. (2) An optimal switching time that occurs soon after a sharp increase in the number of individuals passing through the end of the sensitive period causes the most distinct optimum. (3) Early emergence from diapause (assuming a suitable environment) increases fitness, but neither the mean nor the variance of the distribution of emergence times affects the position of the optimal switching time. (4) Net fecundity, acting through the age distribution, can greatly influence the shape of the fitness function. (5) Populations with fecundity schedules of short duration relative to the length of the juvenile phase are likely to have fitness functions with plateaus and no distinct optimum, depending on the relationship between temporal changes in age structure and the predicted position of the optimum. The width of such plateaus diminishes as the variance of the emergence distribution increases.     

Contrasting life history strategies of sympatric Arctic charr morphs, Salvelinus alpinus

In polymorphic populations morphs usually diverge in morphology, ecology and life history, which is most likely driven by adaptations to different environments or resources. Sympatric morphs may develop differences in several life history traits to be able to maximize fitness in alternative niches and habitats. Here, the contrasting life history traits of three sympatric Arctic charr (Salvelinus alpinus (L.)) morphs in a deep and oligotrophic lake in sub-arctic Norway are addressed. The charr morphs differ in spawning habitat and trophic niche. One is a littoral spawning morph that feeds on benthic invertebrates and zooplankton in the littoral and pelagic zones (referred to as the LO-morph), and two other are profundal spawning morphs that either utilize profundal soft bottom benthos as food resource (the PB-morph) or are piscivorous (the PP-morph). The LO-morph typically had intermediate life-history traits relative to the two profundal morphs that had highly contrasting life history traits, especially in growth and age and size of maturity. The PB-morph matured at a young age (～3 years) and at a small body size (～8.5 cm), thereby increasing their fitness by investing in reproduction early in life, which results in a short generation time and decreased probability of being predated before first reproduction. The PP-morph on the other hand, matured at an old age (～9.2 years) and a large body size (～26 cm), thereby increasing their fitness by investing in somatic growth to enhance initial fecundity, and also to reach a large body size profitable for piscivory. The different trade-off regime between the PP- and PB-morphs seems to be caused by adaptation to alternative trophic niches, and appears to be an important factor for the co-occurrence of the two sister-morphs in the profundal zone.     

Conflicting selection on the timing of germination in a natural population of Arabidopsis thaliana

The timing of germination is a key life‐history trait that may strongly influence plant fitness and that sets the stage for selection on traits expressed later in the life cycle. In seasonal environments, the period favourable for germination and the total length of the growing season are limited. The optimal timing of germination may therefore be governed by conflicting selection through survival and fecundity. We conducted a field experiment to examine the effects of timing of germination on survival, fecundity and overall fitness in a natural population of the annual herb Arabidopsis thaliana in north‐central Sweden. Seedlings were transplanted at three different times in late summer and in autumn covering the period of seed germination in the study population. Early germination was associated with low seedling survival, but also with high survival and fecundity among established plants. The advantages of germinating early more than balanced the disadvantage and selection favoured early germination. The results suggest that low survival among early germinating seeds is the main force opposing the evolution of earlier germination and that the optimal timing of germination should vary in space and time as a function of the direction and strength of selection acting during different life‐history stages.     

Maladaptive Habitat Use of a North American Woodpecker in Population Decline

Rapid anthropogenic habitat changes can lead to non‐ideal habitat use by animals, often resulting in lower fitness and population declines. An extreme case of use and fitness mismatch is an ecological trap where habitat quality cues are disjointed from the true quality of the habitat. Species primarily associated with anthropogenically altered habitat, such as red‐headed woodpeckers (Melanerpes erythrocephalus), may be especially vulnerable to use and fitness mismatch as they encounter novel environmental challenges. We investigated multi‐scale habitat use and nesting success of red‐headed woodpeckers to assess their vulnerability to mismatches between use and fitness as a result of non‐ideal habitat use across multiple scales. We found that habitat characteristics that promote feeding potential such as canopy openness and greater dead limb length appeared paramount and were consistent in use across several spatial scales although reproductive fitness suffered. This contrasts with the assumption that habitat use by nesting birds should instead favor predation avoidance at smaller scales to improve reproductive fitness and suggests that maladaptive, food‐based habitat use by red‐headed woodpeckers in southern Ontario may result in ecological traps for the species. Whether due to poor habitat choices or costly ones in favor of feeding potential, it is vital to consider this behavior in conservation and management plans for this and similar species. We suggest multi‐scale habitat use studies that consider fitness outcomes are critical for species‐at‐risk in human‐modified landscapes.     

Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

Poor conditions during early development can initiate trade‐offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life‐history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early‐life conditions to lifespan and fitness. In wild purple‐crowned fairy‐wrens, we combined measurements of nestling telomere length (TL) with detailed life‐history data to investigate whether early‐life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age‐dependent with early‐life TL having a positive effect on lifespan only among individuals that survived their first year. Early‐life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early‐life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early‐life TL, which reflects growth, accumulated early‐life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early‐life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early‐ and late‐life performance and trade‐offs across a lifetime.     

Detecting Heterogeneity of Substitution along DNA and Protein Sequences

Regions of differing constraint, mutation rate or recombination along a sequence of DNA or amino acids lead to a nonuniform distribution of polymorphism within species or fixed differences between species. The power of five tests to reject the null hypothesis of a uniform distribution is studied for four classes of alternate hypothesis. The tests explored are the variance of interval lengths; a modified variance test, which includes covariance between neighboring intervals; the length of the longest interval; the length of the shortest third-order interval; and a composite test. Although there is no uniformly most powerful test over the range of alternate hypotheses tested, the variance and modified variance tests usually have the highest power. Therefore, we recommend that one of these two tests be used to test departure from uniformity in all circumstances. Tables of critical values for the variance and modified variance tests are given. The critical values depend both on the number of events and the number of positions in the sequence. A computer program is available on request that calculates both the critical values for a specified number of events and number of positions as well as the significance level of a given data set.     

Ontogenetic shifts in habitat use by the endangered Roanoke logperch (Percina rex)

1. Conservation of the federally endangered Roanoke logperch (Percina rex, Jordan and Evermann) necessitates protection of habitat that is critical for all age classes. We examined habitat use patterns of individual logperch to determine: (1) if age classes of logperch in the Nottoway and Roanoke Rivers exhibit habitat selectivity, (2) if age classes differ in habitat use, and (3) if ontogenetic patterns of habitat use differ between the Roanoke and Nottoway river populations. 2. In the summers of 2000 and 2001, we observed 17 young‐of‐year (YOY) logperch [<4 cm total length (TL)], 13 subadult logperch (4–8 cm TL), and 49 adult logperch (>8 cm TL) in the upper Roanoke River, and 40 subadult and 39 adult logperch in the Nottoway River, Virginia. 3. All size classes of Roanoke logperch demonstrated habitat selectivity and logperch used a wide range of habitats in the Roanoke and Nottoway rivers during ontogeny. Habitat use by logperch varied among age classes and between rivers. 4. In the Roanoke River, adult and subadult logperch primarily preferred run and riffle habitat, often over gravel substrate. Subadults were found in lower water velocities and slightly more embedded microhabitats than adults. YOY logperch were found in shallow, stagnant backwaters and secondary channels. In the Nottoway River, both adult and subadult logperch were found over sand and gravel in deep, low‐velocity pools and runs. Subadults were observed in slightly more silted, lower velocity habitat than adults. Shifts in habitat use were more distinct between age classes in the Roanoke River than the Nottoway River. 5. Successful conservation of this species will involve sound understanding of spatial variation in habitat use over logperch life history and preservation of the ecological processes that preserve required habitat mosaics.     

Evolutionary optimization of life-history traits in the sea beet Beta vulgaris subsp. maritima: Comparing model to data

At evolutionary equilibrium, ecological factors will determine the optimal combination of life-history trait values of an organism. This optimum can be assessed by assuming that the species maximizes some criterion of fitness such as the Malthusian coefficient or lifetime reproductive success depending on the degree of density-dependence. We investigated the impact of the amount of resources and habitat stability on a plant's age at maturity and life span by using an evolutionary optimization model in combination with empirical data. We conducted this study on sea beet, Beta vulgaris subsp. maritima, because of its large variation in life span and age at first reproduction along a latitudinal gradient including considerable ecological variation. We also compared the consequence in our evolutionary model of maximizing either the Malthusian coefficient or the lifetime reproductive success. Both the data analysis and the results of evolutionary modeling pointed to habitat disturbance and resources like length of the growing season as factors negatively related to life span and age at maturity in sea beet. Resource availability had a negative theoretical influence with the Malthusian coefficient as the chosen optimality criterion, while there was no influence in the case of lifetime reproductive success. As suggested by previous theoretical work the final conclusion on what criterion is more adequate depends on the assumptions of how in reality density-dependence restrains population growth. In our case of sea beet data R₀ seems to be less appropriate than λ.     

Grandmothering and natural selection

Humans are unique among primates in that women regularly outlive their reproductive period by decades. The grandmother hypothesis proposes that natural selection increased the length of the human post-menopausal period—and, thus, extended longevity—as a result of the inclusive fitness benefits of grandmothering. However, it has yet to be demonstrated that the inclusive fitness benefits associated with grandmothering are large enough to warrant this explanation. Here, we show that the inclusive fitness benefits are too small to affect the evolution of longevity under a wide range of conditions in simulated populations. This is due in large part to the relatively weak selection that applies to women near or beyond the end of their reproductive period. However, we find that grandmothers can facilitate the evolution of a shorter reproductive period when their help decreases the weaning age of their matrilineal grandchildren. Because selection favours a shorter reproductive period in the presence of shorter interbirth intervals, this finding holds true for any form of allocare that helps mothers resume cycling more quickly. We conclude that while grandmothering is unlikely to explain human-like longevity, allocare could have played an important role in shaping other unique aspects of human life history, such as a later age at first birth and a shorter female reproductive period.     

Life histories as adaptive strategies

Optimal control theory is used to produce a general model of life history evolution in a stationary environment. Several disparate trends in current theorizing on life histories are thereby unified. An optimal life history (OLH) is defined as one which maximizes individual fitness (the Malthusian parameter in density-independent populations, the carrying capacity in density-dependent ones). Since the components of fitness depend on the phenotype, the search for an OLH is accomplished in phenotypic space. The optimization is controlled by apportioning the energy obtained at any age between conflicting processes of growth, survival and reproduction. The methods of dynamic optimization which pertain to this problem are reviewed briefly, and its results interpreted biologically. Of these, Pontryagin's method is selected and used to examine some simple models. This method leads one to define a dual variable matched to each phenotypic variable, the prospective value. This provides an indicator of the selective pressures acting at any age on a phenotypic feature to push it towards coincidence with the OLH. This also suggests that at ages in which these dual variables are low (i.e. late ages) there will be greater phenotypic variability around the OLH in any population. The problem of the optimal distribution of reproductive effort over the life history is discussed as well.     

Can pellet counts be used to accurately describe winter habitat selection by moose <Emphasis Type="Italic">Alces alces</Emphasis>?

Pellet counts have been used to measure habitat selection of a variety of ungulate species often under the assumption that this method gives an unbiased sample of the true distribution of the species among habitats. The validity of this method has been questioned and comparisons with other methods have sometimes showed divergent results. We tested the validity of pellet group distribution as a tool for habitat selection studies by comparing the distribution of moose pellet groups in four different forest age categories (forest age <30, 31–60, 61–90, >90 years) and mire with GPS positions from collared moose (Alces alces). Sample plots (n = 531) were cleaned from pellet during the fall 2007 and the number of new pellet groups were counted in spring 2008, thus resulting in a defined period of accumulation. In addition, pellet groups were counted in paired, uncleaned, control plots. GPS data from 15 collared moose monitored during the same period were used for comparison with habitat composition and distribution of pellet groups. Both the distribution of pellet groups and GPS positions differed significantly from the habitat composition within the study area. Young forest stands (<30 years) were significantly more used than both forests >30 years and mire. The selection by moose, as calculated by Manly’s alpha, showed identical ranking among habitat classes for cleaned sample plots and GPS data whereas uncleaned plots showed a shifted rank order for two of the habitat classes. We conclude that pellet group counts can be used to accurately predict habitat use for moose during winter.     

Density-dependent effects of mortality on the optimal body size to shift habitat: Why smaller is better despite increased mortality risk

Many animal species across different taxa change their habitat during their development. An ontogenetic habitat shift enables the development of early vulnerable-to-predation stages in a safe “nursery” habitat with reduced predation mortality, whereas less vulnerable stages can exploit a more risky, rich feeding habitat. Therefore, the timing of the habitat shift is crucial for individual fitness. We investigate the effect that size selectivity in mortality in the rich feeding habitat has on the optimal body size at which to shift between habitats using a population model that incorporates density dependence. We show that when mortality risk is more size dependent, it is optimal to switch to the risky habitat at a smaller rather than larger body size, despite that individuals can avoid mortality by staying longer in the nursery habitat and growing to safety in size. When size selectivity in mortality is high, large reproducing individuals are abundant and produce numerous offspring that strongly compete in the nursery habitat. A smaller body size at habitat shift is therefore favored because strong competition reduces growth potential. Our results reveal the interdependence among population structure, density dependence, and life history traits, and highlight the need for integrating ecological feedbacks in the study of life history evolution.     

Disentangling the Evolution of Early and Late Life History Traits in Humans

Some aspects of human life history are unique among primates. Most notably, humans have a younger weaning age, a later age at first parturition, a shorter female reproductive period, and a longer lifespan than other living hominoid species. Obtaining a better understanding of when and how life history changed during human evolution is important to those studying the evolutionary developmental biology of extinct hominins, as life history traits pace developmental processes. Life history traits are thought to be linked via tradeoffs, such that changes in early life history traits directly affect those that follow later in life, and vice versa. However, it is also worth considering how changes to a single life history trait may indirectly affect other traits by way of modifying selective pressures acting on individuals and groups. For example, because they affect the size and demographic structure of a group, late life history traits (e.g., lifespan) may also affect the evolution of life history traits that occur earlier in life, but by modifying selective pressures acting on juveniles rather than by triggering a physiological tradeoff. This review marks an effort to begin to disentangle the ways in which early and late life history traits may affect each other both directly and indirectly. We concentrate on female life history characteristics. First, we review previous research on the evolution of the postmenopausal lifespan in women. Next we discuss recent findings concerning the relationship between the optimal length of the female reproductive period, mortality, and weaning age that show that selection favors a shorter female reproductive period in the presence of a younger weaning age. We discuss the implications this finding holds for understanding the evolution of life history traits that are of particular interest to developmental biologists.     

Modeling host-associating microbes under selection

The concept of fitness is often reduced to a single component, such as the replication rate in a given habitat. For species with multi-step life cycles, this can be an unjustified oversimplification, as every step of the life cycle can contribute to the overall reproductive success in a specific way. In particular, this applies to microbes that spend part of their life cycles associated to a host. In this case, there is a selection pressure not only on the replication rates, but also on the phenotypic traits associated to migrating from the external environment to the host and vice-versa (i.e., the migration rates). Here, we investigate a simple model of a microbial lineage living, replicating, migrating and competing in and between two compartments: a host and an environment. We perform a sensitivity analysis on the overall growth rate to determine the selection gradient experienced by the microbial lineage. We focus on the direction of selection at each point of the phenotypic space, defining an optimal way for the microbial lineage to increase its fitness. We show that microbes can adapt to the two-compartment life cycle through either changes in replication or migration rates, depending on the initial values of the traits, the initial distribution across the two compartments, the intensity of competition, and the time scales involved in the life cycle versus the time scale of adaptation (which determines the adequate probing time to measure fitness). Overall, our model provides a conceptual framework to study the selection on microbes experiencing a host-associated life cycle.Subject terms: Microbial ecology, Symbiosis, Theoretical ecology, Evolution, Microbiome     

Natural selection of life history attributes: An analytical approach

The life history attributes which maximize fitness can be established analytically through Fisher's equation for reproductive value. Maximizing the reproductive value at age zero is equivalent to maximizing the ultimate rate of increase. As an example of the usefulness of this equality it is shown that when survivorship is uniformly reduced, the corresponding optimal maternal frequency is unaltered, even though the ultimate rate of increase is lowered by a known amount. A general life history model is proposed which links these demographic determinants of rate of increase with the energy utilization alternatives (as among maintenance, growth, and reproduction) characterizing an individual organism's development. Since the energy partitioning alternatives at any age may depend on previous allocations, an organism state variable is introduced to describe the domain over which the maximization of reproductive value may take place. Further, if the reproductive value is to be a maximum at age zero, it must be maximized at every age. An optimal life history, then, is characterized by the energy allocations which maximize sequential reproductive values. Further examples of the utility of the model focus on growth vs reproduction decisions under biomass specific life history attributes. It is shown that if births per unit energy is a linear or convex function, then an organism will not simultaneously grow and reproduce. Determinant growth, biomass at first reproduction, and explicit calculation of the maximum ultimate rate of increase are also illustrated.     

Delayed motherhood decreases life expectancy of mouse offspring

This study analyzes the long-term effects of delayed motherhood on reproductive fitness and life expectancy of offspring in the mouse. Hybrid (C57BL/6JIco x CBA/JIco) first-generation (F1) females, either at the age of 10 or 51 wk, were individually housed with a randomly selected 12- to 14-wk-old hybrid male following a breeding pen system until females reached the end of their reproductive life. Reproductive fitness of second-generation (F2) females was tested from the age of 25 wk until the end of their reproductive life. In F2 males, the testing period ranged from the age of 52 wk until their natural death. Delayed motherhood of hybrid F1 female mice was associated with a decreased percentage of male F3 offspring at birth and lower life expectancy and body weight during adulthood of F2 offspring. There was, however, no evident negative effect of delayed motherhood on several reproductive fitness variables in either male or female F2 offspring. This included between-parturition interval, litter size at birth and at weaning, body weight at weaning and preweaning mortality of F3 pups, percentage of F3 litters with at least one pup cannibalized, and time at which female and male F2 offspring ceased their reproductive life. These data clearly show that delayed motherhood in the mouse is associated with negative long-term effects on offspring survival.     

秦岭北坡栓皮栎种群动态的研究

对秦岭北坡栓皮栎种群动态进行了系统研究,分析了种群的年龄结构和分布格局。编制了静态生命表。绘制了存活曲线．结果表明,秦岭北坡栓皮栎种群年龄结构属于进展型,幼龄个体多。中老龄个体少;种群在I、Ⅱ龄级时死亡率最高．随着年龄增加,死亡率逐渐降低;到Ⅶ、Ⅷ龄级。由于生理衰老。死亡率回升;栓皮栎种群存活曲线属于DeeveyⅢ型;种群分布格局总体上的呈聚集型。随年龄增加,种群聚集强度降低。在高海拔地区,种群趋向随机分布．海拔800～1100m是栓皮栎种群较为适宜的生境．对于低海拔地区栓皮栎林要加强保护,减少人为干扰;中海拔地区应加强抚育管理和适时间伐,高海拔地区应加强目的树种的抚育．     

A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus)

1. Long-term effects of conditions during early development on fitness are important for life history evolution and population ecology. Using multistrata mark-recapture models on 20 years of data, we quantified the relation between rearing conditions and lifetime fitness in a long-lived shorebird, the oystercatcher (Haematopus ostralegus). We addressed specifically the relative contribution of short- and long-term effects of rearing conditions to overall fitness consequences. 2. Rearing conditions were defined by differences in natal habitat quality, in which there is a clear dichotomy in our study population. In the first year of life, fledglings from high-quality natal origin had a 1.3 times higher juvenile survival. Later in life (age 3-11), individuals of high-quality natal origin had a 1.6 times higher adult prebreeder survival. The most striking effect of natal habitat quality was that birds that were reared on high-quality territories had a higher probability of settling in high-quality habitat (44% vs. 6%). Lifetime reproductive success of individuals born in high-quality habitat was 2.2 times higher than that of individuals born in low-quality habitat. This difference increased further when fitness was calculated over several generations, due to a correlation between the quality of rearing conditions of parents and their offspring. 3. Long-term effects of early conditions contributed more to overall fitness differences as short-term consequences, contrary to common conceptions on this issue. 4. This study illustrates that investigating only short-term effects of early conditions can lead to the large underestimation of fitness consequences. We discuss how long-term consequences of early conditions may affect settlement decisions and source-sink population interactions.