A new demographic function maximized by life-history evolution

A goal of life-history theory has been to understand what combination of demographic traits is maximized by natural selection. In practice, researchers usually choose either density-independent population growth rate, lambda, or lifetime reproductive success, R0 (expected number of offspring produced in a lifetime). Others have shown that the maxima of density-independent lambda and R0 are evolutionarily stable strategies under specific density-dependent conditions: population regulation by equal density dependence among all age classes for lambda and by density dependence on a single age class for R0. Here I extend these connections between density-independent optimization models and density-dependent invasion function models in two ways. First, I derive a new demographic function for which a maximum corresponds to attainability of the equilibrium strategy or stability of the mean rather than stability of the variance of the strategy distribution. Second, I show explicitly a continuous range of cases with maxima between those for the lambda and R0. Graphical and biological interpretations are given for an example model. Finally, exceptions to a putative life-history generality (from lambda and R0 models), that high early-life mortality selects for high iteroparity, are shown.     

Density dependence, lifespan and the evolutionary dynamics of longevity

Longevity is a life-history trait that is shaped by natural selection. Evolution will shape mortality trajectories and lifespans, but until now the evolutionary analysis of longevity is based principally on a density-independent (Euler-Lotka) framework. The effects of density dependence on the evolution of lifespan and mortality remain largely unexplored. We investigate the influence of different population demographies on the evolution of longevity, and show how these can be linked to adaptive radiations. We present a range of models to explore the intraspecific and interspecific density effects on longevity and, consequently, diversification. We show how the magnitude, type, and timing of mutation can also affect fitness, invasion and diversification. We argue that fitness of alternative strategies under a range of different demographic structures leads to flat, as opposed to rugged, landscapes and that these flat fitness surfaces are important in the evolution of lifespan and senescence.     

Factors influencing detection of density dependence in British birds

If censuses are taken at less than generation intervals, the number of successive censuses in which a given individual is recorded will depend on longevity. Repeatedly recording the same individuals could produce under-estimates of population variability and influence detection of density dependence. We investigated this possibility in 60 time series of abundances of British birds compiled from the Common Birds Census data and then used simple population models to illustrate the proposed mechanism. Species had average lifespans of 2–10 years and were censused annually. Density dependence was detected (at P<0.05) much more frequently in bird species with long lifespans than in those with short lifespans; 75% of the 12 longest-lived species showed density dependence compared to 46% of all species. Population variability measured in annual censuses (termed annual variability) was lower in bird species with longer lifespans. We used discrete time models based on difference equations to demonstrate how longevity influences population variability and detection of density dependence in series of annual censuses. A model in which only first-year birds experienced density dependence was rejected because annual variability was greater and detection of density dependence was less likely when longevity was greater, the opposite of the observed effects of longevity in birds. A model in which all age classes experienced density dependence gave time series with lower annual variability and in which density dependence was detected more frequently when longevity was greater, which is the pattern observed in British birds. Analysis of data from this model showed that the amount of density dependence actually present caused only small changes in annual variability, whereas detection of density dependence from simulated series was strongly influenced by annual variability. The high annual variability of series from short-lived bird species could mask any density dependence that was present. Correcting for trends lead us to detect density dependence in 75% of the 12 longest lived bird species. There is no reason to believe that this rate is not also representative of short-lived species.     

Individual heterogeneity in life-history trade-offs with age at first reproduction in capital breeding elephant seals

Recruitment age plays a key role in life-history evolution. Because individuals allocate limited resources among competing life-history functions, theory predicts trade-offs between current reproduction and future growth, survival and/or reproduction. Reproductive costs tend to vary with recruitment age, but may also be overridden by fixed individual differences leading to persistent demographic heterogeneity and positive covariation among demographic traits at the population level. We tested for evidence of intra- and inter-generational trade-offs and individual heterogeneity relating to age at first reproduction using three decades of detailed individual life-history data of 6,439 capital breeding female southern elephant seals. Contrary to the predictions from trade-off hypotheses, we found that recruitment at an early age was associated with higher population level survival and subsequent breeding probabilities. Nonetheless, a survival cost of first reproduction was evident at the population level, as first-time breeders always had lower survival probabilities than prebreeders and experienced breeders of the same age. However, models accounting for hidden persistent demographic heterogeneity revealed that the trade-off between first reproduction and survival was only expressed in “low quality” individuals, comprising 35% of the population. The short-term somatic costs associated with breeding at an early age had no effect on the ability of females to allocate resources to offspring in the next breeding season. Our results provide strong evidence for individual heterogeneity in the life-history trajectories of female elephant seals. By explicitly modeling hidden persistent demographic heterogeneity we show that individual heterogeneity governs the expression of trade-offs with first reproduction in elephant seals.     

Life-history correlates of maximum population growth rates in marine fishes

Theory predicts that populations of animals with late maturity, low fecundity, large body size and low body growth rates will have low potential rates of population increase at low abundance. If this is true, then these traits may be used to predict the intrinsic rate of increase for species or populations, as well as extinction risks. We used life-history and population data for 63 stocks of commercially exploited fish species from the northeast Atlantic to test relationships between life-history parameters and the rate of population increase at low abundance. We used cross-taxonomic analyses among stocks and among species, and analyses that accounted for phylogenetic relationships. These analyses confirmed that large-bodied, slow-growing stocks and species had significantly lower rates of recruitment and adult production per spawning adult at low abundance. Furthermore, high ages at maturity were significantly correlated with low maximum recruit production. Contrary to expectation, fecundity was significantly negatively related to recruit production, due to its positive relationship with maximum body size. Our results support theoretical predictions, and suggest that a simply measured life-history parameter can provide a useful tool for predicting rates of recovery from low population abundance.     

Growth of female southern elephant seals Mirounga leonina at Macquarie Island

Body growth of 137 female southern elephant seals (Mirounga leonina) over 1 year of age was investigated at subantarctic Macquarie Island. An asymptotic straight line, snout–tail body length of 2.57±0.03 m was estimated to be attained at 9 years of age, using a three-parameter Gompertz equation. A significant increase of approximately 0.1 m (5%) in mean body length of females between 1 and 10 years of age was estimated to have occurred between the 1950–1960s and 1990s at Macquarie Island. This is consistent with a reduction in both the rate of population decline and the age of onset of sexual maturity. Age determination using dental cementum layers and the importance of standardised measurements in pinniped growth studies are discussed.     

Deep-sea fishes in Canada’s Atlantic: population declines and predicted recovery times

Because of their slow growth rates, late maturity, low fecundity and long potential lifespans, deep-sea fishes are vulnerable to and theoretically slow to recover from overexploitation and bycatch. As industrial fishing moved into the deep sea, population declines were predicted and five species were shown to meet The World Conservation Union (IUCN) criteria for endangered species in Atlantic Canadian waters and two other deep-living species were listed as threatened by the Committee on the Status of Endangered Wildlife in Canada. We used data from scientific surveys to determine population trends in a 17-year time series for an additional 32 deep-sea fishes from the same geographic region. Eight species exhibited significant population declines, five increased, two were data deficient, and 17 showed no significant trends. Thus approximately 38% of the deep-sea bottom-living fishes in that well-investigated region could be at-risk, but definitive assignment to an IUCN category for most species is hampered by a lack of basic biological information, especially species specific generation times. Lack of biological information also limits efforts to determine possible recovery times, especially with respect to calculating intrinsic rates of population growth (r). For two Atlantic grenadiers (where r could be estimated using life-history parameters and standard life table techniques), the time to recovery with no fishing mortality could range from over a decade to over a century. This broad range results from the general uncertainty on life-history characteristics of these deep-sea species. Given the documented declines, the lack of basic data on life-history parameters, and the conservative assumption that recovery rates are likely to be prolonged, we argue that it is imperative to conduct additional studies pertaining to life history characteristics of deep-sea fishes and implement conservation measures in the deep sea immediately.     

Comparing growth patterns among field populations of cereal aphids reveals factors limiting their maximum abundance

Cereal stands in central Europe are commonly infested with three species of aphids that may become serious pests. With increasing abundance, the proportion of a particular species in the total aphid population may remain constant, suggesting a density-independent exponential growth, or the proportion can change, suggesting density-dependent constraints on growth. The constraints that affect particular species, and thus their relative abundance, were studied. The proportionality between maximum abundances of the cereal aphids was studied using a 10-year census of the numbers of aphids infesting 268 winter wheat plots. For two species their abundance on leaves and ears was compared. With increasing aphid density the maximum abundance of Rhopalosiphum padi (Linnaeus) remained proportional, but not that of Sitobion avenae (Fabricius), which was constrained by the smaller surface area of ears compared to leaves. There was no evidence of inter-specific competition. Maximum abundance of R. padi and Metopolophium dirhodum (Walker) on leaves did not change proportionally as the proportion of M. dirhodum decreased with increasing overall aphid density. This decrease was probably caused by the restricted distribution of M. dirhodum, which is confined to leaves, where space is limiting. No change in proportion between populations was detected when the average densities were below 0.54 aphids per leaf or ear. Non-proportional relationships between aphid populations appeared to be due to spatial constraints, acting upon the more abundant population. Detecting the limitation of population growth can help with the assessment of when density-independent exponential growth is limited by density-dependent factors. This information may help in the development of models of cereal aphid population dynamics.     

Estimating density dependence in time-series of age-structured populations

For a life history with age at maturity alpha, and stochasticity and density dependence in adult recruitment and mortality, we derive a linearized autoregressive equation with time-lags of from 1 to alpha years. Contrary to current interpretations, the coefficients for different time-lags in the autoregressive dynamics do not simply measure delayed density dependence, but also depend on life-history parameters. We define a new measure of total density dependence in a life history, D, as the negative elasticity of population growth rate per generation with respect to change in population size, D = - partial differential lnlambda(T)/partial differential lnN, where lambda is the asymptotic multiplicative growth rate per year, T is the generation time and N is adult population size. We show that D can be estimated from the sum of the autoregression coefficients. We estimated D in populations of six avian species for which life-history data and unusually long time-series of complete population censuses were available. Estimates of D were in the order of 1 or higher, indicating strong, statistically significant density dependence in four of the six species.     

Phylogenetic prediction of the maximum per capita rate of population growth

The maximum per capita rate of population growth, r, is a central measure of population biology. However, researchers can only directly calculate r when adequate time series, life tables and similar datasets are available. We instead view r as an evolvable, synthetic life-history trait and use comparative phylogenetic approaches to predict r for poorly known species. Combining molecular phylogenies, life-history trait data and stochastic macroevolutionary models, we predicted r for mammals of the Caniformia and Cervidae. Cross-validation analyses demonstrated that, even with sparse life-history data, comparative methods estimated r well and outperformed models based on body mass. Values of r predicted via comparative methods were in strong rank agreement with observed values and reduced mean prediction errors by approximately 68 per cent compared with two null models. We demonstrate the utility of our method by estimating r for 102 extant species in these mammal groups with unknown life-history traits.     

Variability in temporary emigration rates of individually marked female Weddell seals prior to first reproduction

In many species, temporary emigration (TE) is a phenomenon, often indicative of life-history characteristics such as dormancy, skipped reproduction, or partial migration, whereby certain individuals in a population are temporarily unobservable at a particular site. TE may be a flexible condition-dependent strategy that allows individuals to mitigate effects of adverse conditions. Consequently, TE rates ought to be highly variable, but sources of variations are poorly understood for most species. We used data from known-aged female Weddell seals (Leptonychotes weddellii) tagged in Erebus Bay, Antarctica, to investigate sources of variation in TE rates prior to reproduction and to evaluate possible implications for age-specific probability of first reproduction. TE rates were near 1 the year after birth, decreased to an average of 0.15 ( $ \widehat{\text{SE}} $  = 0.01) by age 8, and were similar thereafter. TE rates varied substantially from year-to-year and were lower for seals that attended reproductive colonies the previous year than for seals that did not attend (e.g., $ \overline{{\hat{\psi }_{{i,{\text{age}}\,8}}^{\text{UU}} - \hat{\psi }_{{i,\,{\text{age}}\,8}}^{\text{PU}} }} $  = 0.22). Recruitment rates were marginally greater for seals that did attend than for seals that did not attend colonies the previous year. For Weddell seals specifically, our results suggest that (1) motivation to attend colonies varied temporally, (2) as seals grew older they had increased motivation to attend even before reproductive maturity, and (3) seals appear to follow various attendance strategies. More broadly, our results support the idea of TE as a variable, condition-dependent strategy, and highlight the utility of TE models for providing population and life-history insights for diverse taxa.     

Mitochondrial DNA structure and colony expansion dynamics of New Zealand fur seals (Arctocephalus forsteri) around Banks Peninsula

New Zealand fur seals are one of many pinniped species that survived the commercial sealing of the eighteenth and nineteenth centuries in dangerously low numbers. After the enforcement of a series of protection measures in the early twentieth century, New Zealand fur seals began to recover from the brink of extinction. We examined the New Zealand fur seal populations of Banks Peninsula, South Island, New Zealand using the mitochondrial DNA control region. We identified a panmictic population structure around Banks Peninsula. The most abundant haplotype in the area showed a slight significant aggregated structure. The Horseshoe Bay colony showed the least number of shared haplotypes with other colonies, suggesting a different origin of re-colonisation of this specific colony. The effective population size of the New Zealand fur seal population at Banks Peninsula was estimated at approximately 2500 individuals. The exponential population growth rate parameter for the area was 35, which corresponds to an expanding population. In general, samples from adjacent colonies shared 4.4 haplotypes while samples collected from colonies separated by between five and eight bays shared 1.9 haplotypes. The genetic data support the spill-over dynamics of colony expansion already suggested for this species. Approximate Bayesian computations analysis suggests re-colonisation of the area from two main clades identified across New Zealand with a most likely admixture coefficient of 0.41 to form the Banks Peninsula population. Approximate Bayesian computations analysis estimated a founder population size of approximately 372 breeding individuals for the area, which then rapidly increased in size with successive waves of external recruitment. The population of fur seals in the area is probably in the late phase of maturity in the colony expansion dynamic.     

The case for negative senescence

Negative senescence is characterized by a decline in mortality with age after reproductive maturity, generally accompanied by an increase in fecundity. Hamilton (1966) ruled out negative senescence: we adumbrate the deficiencies of his model. We review empirical studies of various plants and some kinds of animals that may experience negative senescence and conclude that negative senescence may be widespread, especially in indeterminate-growth species for which size and fertility increase with age. We develop optimization models of life-history strategies that demonstrate that negative senescence is theoretically possible. More generally, our models contribute to understanding of the evolutionary and demographic forces that mold the age-trajectories of mortality, fertility and growth.     

Morphometric variation in the Hooded seal (Cystophora cristata)

Intra- and intersexual variation in 16 skull dimensions and total body length of 233 aged Hooded seals caught in the north-west Atlantic were investigated. Absolute growth was described by asymptotic growth curves applied to single dimensions, as well as to scores on the first principal component of logarithmically transformed cranial data, which are believed to reflect the multivariate nature of growth. All dimensions were found to be fully developed later in males than in females. The growth of the male skulls was found to continue for more than 20 years, while the females approach final size about–7 years earlier than males, according to the scores on the first principal component. Female seals were found to reach 86 % of final total body length at the time of maturation, which is a generalized pinniped pattern. In both sexes, a yearling skull was characterized by a large brain-case, which decreased relatively with growth. The male skulls were further characterized by an increase in zygomatic width and orbital width in relation to basal length, a pattern which was not found in females.
All the asymptotic values were significantly larger in males than in females. The dimorphism develops mainly as a result of prolonged growth of males after the attainment of sexual maturity.     

TRENDS IN ABUNDANCE AND CURRENT STATUS OF HARBOR SEALS IN OREGON: 1977–2003

The distribution and abundance of harbor seals ( Phoca vitulina richardii ) in Oregon were monitored from 1977 to 2003 by aerial photographic surveys. Harbor seals on shore were counted each year during the reproductive period. Mean annual counts of non-pups (adults and subadults) were used as an index of population size and the trend in the counts was modeled using exponential (density-independent) and generalized logistic (density-dependent) growth models. Models were fit using maximum likelihood and evaluated using Akaike's Information Criterion. The population dynamics of harbor seals in Oregon were best described by the generalized logistic model. The population grew following protection under the Marine Mammal Protection Act of 1972 until stabilizing in the early 1990s. The estimated absolute abundance of harbor seals (all age classes) during the 2002 reproductive period was 10,087 individuals (95% confidence interval was 8,445–12,046 individuals). The current predicted population size for harbor seals in Oregon is above its estimated maximum net productivity level and hence within its optimum sustainable population range. We speculate that recent increases in ocean productivity in the eastern Pacific Ocean may lead to an increase in carrying capacity and renewed growth in Oregon's harbor seal population.     

Bridging Developmental Boundaries: Lifelong Dietary Patterns Modulate Life Histories in a Parthenogenetic Insect

Determining the effects of lifelong intake patterns on performance is challenging for many species, primarily because of methodological constraints. Here, we used a parthenogenetic insect (Carausius morosus) to determine the effects of limited and unlimited food availability across multiple life-history stages. Using a parthenogen allowed us to quantify intake by juvenile and adult females and to evaluate the morphological, physiological, and life-history responses to intake, all without the confounding influences of pair-housing, mating, and male behavior. In our study, growth rate prior to reproductive maturity was positively correlated with both adult and reproductive lifespans but negatively correlated with total lifespan. Food limitation had opposing effects on lifespan depending on when it was imposed, as it protracted development in juveniles but hastened death in adults. Food limitation also constrained reproduction regardless of when food was limited, although decreased fecundity was especially pronounced in individuals that were food-limited as late juveniles and adults. Additional carry-over effects of juvenile food limitation included smaller adult size and decreased body condition at the adult molt, but these effects were largely mitigated in insects that were switched to ad libitum feeding as late juveniles. Our data provide little support for the existence of a trade-off between longevity and fecundity, perhaps because these functions were fueled by different nutrient pools. However, insects that experienced a switch to the limited diet at reproductive maturity seem to have fueled egg production by drawing down body stores, thus providing some evidence for a life-history trade-off. Our results provide important insights into the effects of food limitation and indicate that performance is modulated by intake both within and across life-history stages.     

Estimating density dependence from population time series using demographic theory and life-history data

For populations with a density-dependent life history reproducing at discrete annual intervals, we analyze small or moderate fluctuations in population size around a stable equilibrium, which is applicable to many vertebrate populations. Using a life history having age at maturity alpha, with stochasticity and density dependence in adult recruitment and mortality, we derive a linearized autoregressive equation with time lags from 1 to alpha yr. Contrary to current interpretations, the coefficients corresponding to different time lags in the autoregressive dynamics are not simply measures of delayed density dependence but also depend on life-history parameters. The theory indicates that the total density dependence in a life history, D, should be defined as the negative elasticity of population growth rate per generation with respect to change in population size, [Formula: see text], where lambda is the asymptotic multiplicative growth rate per year, T is the generation time, and N is adult population size. The total density dependence in the life history, D, can be estimated from the sum of the autoregression coefficients. We estimate D in populations of seven vertebrate species for which life-history studies and unusually long time series of complete population censuses are available. Estimates of D were statistically significant and large, on the order of 1 or higher, indicating strong density dependence in five of the seven species. We also show that life history can explain the qualitative features of population autocorrelation functions and power spectra and observations of increasing empirical variance in population size with increasing length of time series.     

Naked mole-rat and Damaraland mole-rat exhibit lower respiration in mitochondria,cellular and organismal levels

Naked mole-rats (NMR) and Damaraland mole-rats (DMR) exhibit extraordinary longevity for their body size, high tolerance to hypoxia and oxidative stress and high reproductive output; these collectively defy the concept that life-history traits should be negatively correlated. However, when life-history traits share similar underlying physiological mechanisms, these may be positively associated with each other. We propose that one such potential common mechanism might be the bioenergetic properties of mole-rats. Here, we aim to characterize the bioenergetic properties of two African mole-rats. We adopted a top-down perspective measuring the bioenergetic properties at the organismal, cellular, and molecular level in both species and the biological significance of these properties were compared with the same measures in Siberian hamsters and C57BL/6 mice, chosen for their similar body size to the mole-rat species. We found mole-rats shared several bioenergetic properties that differed from their comparison species, including low basal metabolic rates, a high dependence on glycolysis rather than on oxidative phosphorylation for ATP production, and low proton conductance across the mitochondrial inner membrane. These shared mole-rat features could be a result of evolutionary adaptation to tolerating variable oxygen atmospheres, in particular hypoxia, and may in turn be one of the molecular mechanisms underlying their extremely long lifespans.     

Accounting for wildlife life-history strategies when modeling stochastic density-dependent populations: A review

This article briefly reviews and provides discussion on the evidence for, and nature of, density-dependence patterns in r and K-selected species. In this review, I discuss how life-history strategies cause different nonlinear density-dependence patterns and I provide a simple modeling recommendation to incorporate nonlinear density dependence in population growth equations. Second, I discuss the importance of incorporation of environmental stochasticity and local extinction associated with nonlinear density dependence associated with life-history patterns through a novel modeling exercise. Last, I discuss the importance of considering how life-history nonlinear density dependence could affect optimal harvest yields. Though these topics are extensive, this review should spur wildlife biologists and managers to consider more inclusive population models that incorporate life-history strategies and stochasticity in their decision-making processes. © 2012 The Wildlife Society.