Host-parasite coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites.

The environmental factors that drive the evolution of parasite life histories are mostly unknown. Given that hosts provide the principal environmental features parasites have to deal with, and given that these features (such as resource availability and immune responses) are well characterized by the life history of the host, we may expect natural selection to result in covariation between parasite and host life histories. Moreover, some parasites show a high degree of host specificity, and cladistic analyses have shown that host and parasite phylogenies can be highly congruent. These considerations suggest that parasite and host life histories may covary. The central argument in the theory of life history evolution concerns the existence of trade-offs between traits. For parasitic nematodes it has been shown that larger body sizes induce higher fecundity, but this is achieved at the expense of delayed maturity. As high adult mortality would select for reduced age at maturity, the selective benefit of increased fecundity is expressed only if adult mortality is low. Parasite adult mortality may depend on a number of factors, including host longevity. Here we tested the hypothesis concerning the positive covariation between parasite body size (which reflects parasite longevity) and host longevity. To achieve this goal, we used the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Oxyurids are highly host specific and are supposed to be involved in a coevolutionary process with their hosts. We found that female parasite body length was positively correlated with host longevity after correcting for phylogeny and host body mass. Conversely, male parasite body length and host longevity were not correlated. These results confirm that host longevity may represent a constraint on the evolution of body size in oxyurids, at least in females. The discrepancy between female and male oxyurids is likely to depend on the particular mode of reproduction of this taxon (haplodiploidy), which should result in weak (or even null) selection pressures to an increase of body size in males.     

The evolution of life-history traits in parasitic and free-living platyhelminthes: a new perspective

Parasite life histories have been assumed to be shaped by their particular mode of existence. To test this hypothesis, we investigate the relationships between life-history traits of free-living and parasitic platyhelminthes. Using phylogenetically independent contrasts we examine patterns of interspecific covariation in adult size, progeny volume, daily fecundity, total reproductive capacity, age at first reproduction and longevity. The correlations obtained indicate a similar causal chain of life history variations for free-living and parasitic platyhelminthes. These results suggest that increased longevity favours delayed reproduction. Furthermore, growth pattern determines adult body size and age at maturity. For platyhelminthes, whether free-living or parasitic, the total reproductive capacity is found to be directly determined by the size of the worm. Within this group the parasitic way of life does not seem to influence the basic patterns of life history evolution. Received: 20 September 1997 / Accepted: 1 March 1998     

Comparative analysis of phylogenetic and fishing effects in life history patterns of teleost fishes

The effects of fishing on life history traits and life history strategies of teleost fishes are analysed by a new comparative method that splits traits into an allometric part (size effect), an autoregressive phylogenetic component, and an environmental component (fishing effect). Both intra- and inter-specific variation of age and size at maturity, fecundity, adult size and egg size are analysed by comparing 84 populations of 49 species submitted to various fishing pressures. Two axes of life history diversification are found among teleosts. One is the well-known slow-fast continuum separating short-lived and early maturing species (like Clupeiformes) from longer-lived species that mature late relative to their size and spawn larger eggs (like salmonids or Scorpaeniformes). An additional strategy involves the schedule of resource allocation to growth and reproduction. Indeterminate growth allows higher teleosts (e.g. Gadiformes) to reach a large size while maturing early and laying small eggs. Increasing fishing pressure decreases age at maturity and egg size, and increases fecundity at maturity, the slope of the fecundity-length relationship and relative size at maturity. These compensations for higher adult mortality differ among life history strategies. Indeterminate growth is associated with a greater flexibility in resource allocation to growth and reproduction that facilitates greater resilience to fishing mortality.     

Life history characteristics of a lightly exploited stock of Squalus suckleyi

The purpose of this study was to examine the basic life history of a lightly exploited stock of Squalus suckleyi in the Gulf of Alaska to establish a baseline for future comparison and to provide critical information for stock assessments. Average total length (total length extended) of females (87·7 cm) was significantly larger (t-test, t = -12·57, d.f. = 1533, P < 0·01) than males (80·3 cm); size at 50% maturity (74·5 and 97·3 cm, males and females, respectively) and age at 50% maturity (21 and 36 years, respectively) were also significantly different between the sexes (i.e. bootstrapped 95% c.i. did not overlap). Total average fecundity was 8·5 pups per female, and individual fecundity was a linear function of either length or whole mass. The best estimate of instantaneous natural mortality was 0·097. The delayed age of maturity, low natural mortality and low rates of reproduction imply that only very low rates of fishing mortality are sustainable. Finally, this paper provides the first reported evidence that a small percentage of the adult females may undergo an extended resting period between pregnancies of ≥ 1 years.     

The effects of productivity and seasonality on life history: comparing age at maturity among moose (Alces alces) populations

The productivity hypothesis in respect of an animal species’ geographical range predicts that whereas higher productivity at the equatorial periphery of a species’ range favours superior competitors, lower productivity at the centre of a species’ range favours high reproduction and reduced competitive traits. I test whether life‐history patterns follow this hypothesis, using demographic data from 15 Canadian moose (Alces alces) populations. Two models are contrasted; the first assumes that intraspecific variation in age at maturity is explained proximately by density and juvenile mortality. Age at maturity was found to increase with decreasing juvenile mortality (P = 0.01) and increasing density (P = 0.006). To test the productivity hypothesis, the second model additionally included primary productivity and seasonality as geographical explanatory variables that would ultimately influence age at maturity via juvenile mortality and density. Path analysis indicated that including productivity and seasonality improved the model predictions of variation in age at maturity (R_a² 0.56 and 0.85). In bivariate comparisons, seasonality was negatively associated (P = 0.01) with age at maturity. In the best model, however, primary productivity was the environmental variable that explained 25% of the variance in age at maturity, and forest cover replaced seasonality as an explanatory variable. The positive association between primary productivity and age at maturity is consistent with the productivity hypothesis. Relative to populations that lived at the centre of the species’ range (51°N), moose populations living in relatively high productivity and low seasonality environments (equatorial periphery of species’ range; 48°N) experienced less juvenile mortality, more variable year‐to‐year density, higher relative density and slower life history (slower growth rate, later age at maturity, lower fecundity).     

Effects of reproductive mode on demography and life history in Arabis fecunda (Brassicaceae)

Life history theory predicts that trade-offs between growth and reproduction should be dictated by a population's mortality schedule. We tested this prediction with Arabis fecunda, a short-lived perennial that occurs in many different habitats in southwest Montana. Individuals produce either or both axillary or terminal inflorescences. Axillary-flowering plants are usually iteroparous and have smaller reproductive bouts, while terminal-flowering plants have larger reproductive bouts, and tend to be semelparous. We recorded size and fecundity of A. fecunda individuals from 1989 to 1993 in three different habitats. There was great variation in demographic and life history traits among the populations. A wide range of life history strategies among populations of A. fecunda is achieved through different proportions of axillary- and terminal-flowering plants. Arabis fecunda demonstrated a lower recruitment rate, higher survivorship, slower growth, and lower annual fecundity at the low-elevation site compared to the high-elevation site. At the low-elevation site population size was more stable, and elasticity analysis of matrix projection models indicated that adult survivorship was the most important demographic parameter contributing to population growth. This association of life history characters conforms to theoretical predictions.     

Life-history correlates of evolution under high and low adult mortality

Abstract. Life-history theory predicts evolutionary changes in reproductive traits and intrinsic mortality rates in response to differences in extrinsic mortality rates. Trade-offs between life- history traits play a pivotal role in these predictions, and such trade-offs are mediated, at least in part, by physiological allocations. To gain insight into these trade-offs, we have been performing a long-term experiment in which we allow fruitflies, Drosophila melanogaster , to evolve in response to high (HAM) and low (LAM) adult mortality rates. Here we analyze the physiological correlates of the life-history trade-offs. In addition to changing development time and early fecundity in the direction predicted, high adult mortality affected three traits expressed early in life–body size, growth rate, and ovariole number–but had little or no effect on body composition (relative fat content), viability, metabolic rate, activity, starvation resistance, or desiccation resistance. Correlations among lines revealed trade-offs between early fecundity, late fecundity, and starvation resistance, which appear to be mediated by differential allocation of lipids.     

Comparative demography of commercially important parrotfish species from Micronesia

Fishery‐independent sampling was used to determine growth patterns, life span, mortality rates and timing of maturation and sex change in 12 common parrotfishes (Labridae: tribe Scarinae) from five genera (Calotomus, Cetoscarus, Chlorurus, Hipposcarus and Scarus) in Micronesia. Interspecific variation in life‐history traits was explored using multivariate analysis. All species displayed strong sex‐specific patterns of length‐at‐age among which males reached larger asymptotic lengths. There was a high level of correlation among life‐history traits across species. Relationships between length‐based and age‐based variables were weakest, with a tenuous link between maximum body size and life span. Cluster analysis based on similarities among life‐history traits demonstrated that species were significantly grouped at two major levels. The first grouping was driven by length‐based variables (lengths at maturity and sex change and maximum length) and separated the small‐ and large‐bodied species. Within these, species were grouped by age‐based variables (age at maturity, mortality and life span). Groupings based on demographic and life‐history features were independent of phylogenetic relationships at the given taxonomic level. The results reiterate that body size is an important characteristic differentiating species, but interspecific variation in age‐based traits complicates its use as a life‐history proxy. Detailed life‐history metrics should facilitate future quantitative assessments of vulnerability to overexploitation in multispecies fisheries.     

Life-history evolution in uncertain environments: bet hedging in time

Many vertebrates, forest herbs, and trees exhibit both variable age at maturity and iteroparity as adaptations to uncertain environments. We analyze a stochastic model that combines these two life-history adaptations with density-dependent fertility. Results for a model with only iteroparity are consistent with previous work; environmental uncertainty favors adult survival over juvenile survival. This holds true even if there is a moderately strong convex trade-off between adult survival and fecundity, but the direction of selection can depend on which life-history trait is considered a random variable. A life history with only developmental delay favors juvenile survival in uncertain environments, consistent with previous models of seed banks. When both developmental delay and iteroparity are included in the model, both adaptations are favored in uncertain environments. Our simulations show that selection is not necessarily a runaway process in which either developmental delay or iteroparity is favored, as recently proposed by Tuljapurkar and Wiener, but rather that selection can favor both mechanisms. Invasion analysis shows that selective pressure on life-history delays increases as environmental variation increases. Reproductive delay and adult survival can be either adaptations or constraints. Natural-history studies that estimate model parameters can resolve this uncertainty.     

The evolution of fledging age in songbirds

In birds with altricial young an important stage in the life history is the age at fledging. In this paper we use an approach proven successful in the prediction of the optimal age at maturity in fish and reptiles to predict the optimal age of fledging in passerines. Integrating the effects of growth on future fecundity and survival leads to the prediction that the optimal age at fledging is given by a function that comprises survival to maturity, the exponent of the fecundity-body size relationship and nestling growth. Growth is described by the logistic equation with parameters, A, K and t(i). Assuming that the transitional mortality curve can be approximated by the nestling mortality, M(n), the optimal fledging age, t(f), is given by a simple formula involving the three growth parameters, nestling mortality (M(n)) and the exponent (d) of the fecundity-body size relationship. Predictions of this equation underestimate the true values by 11-16%, which is expected as a consequence of the transitional mortality function approximation. A transitional mortality function in which mortality is approximately 0.3-0.4 of nesting mortality (i.e. mortality declines rapidly after fledging) produces predictions which, on average, equal the observed values. Data are presented showing that mortality does indeed decline rapidly upon fledging.     

Evolutionarily stable age at first reproduction in a density-dependent model.

We develop a new model of life history evolution to investigate the evolution of age at first reproduction. Density dependence is taken into account. For a given "species", age of maturity, offspring survival, immature survival, adult survival, fecundity, immature age-classes entering in competition with adults and immature competitive ability are traits adjustable by natural selection, and constitute a particular strategy. On the contrary, the type of intraspecific competition (scramble or contest), strength of competition and inherent net reproductive rate Ro(inh) are fixed (specific) characteristics. As a consequence of fixing Ro(inh), the evolution of any trait will affect trade-offs between others. Evolutionarily stable strategies are determined numerically by using the mathematical concept of Lyapunov exponents. Altogether, we consider 960 different hypothetical "species" (i.e. different combinations of fixed traits). Corresponding ESSs are analyzed with respect to their age at first reproduction, adult survival and immature competitive ability components. They appear to be gathered in three groups. One is intuitive and characterized by a reduction of immature competitive ability and a correlation of age of maturity with adult survival; populations reach mainly equilibria. The two other groups respectively include "species" with low age of maturity but high adult survival, and "species" close to semelparity with delayed maturity; immature competitive ability may not be minimized, and populations possibly exhibit complex dynamics. In conclusion, the hypothesis that the evolution of a demographic parameter modifies trade-offs between others turns out to have important consequences. We argue that life history theory cannot ignore the source and mode-of-operation of density dependence and must regard potential short-term instability as essential.     

Life history patterns in lizards of the arid and semiarid zone of Australia

Summary Studies on the life histories and population dynamics of lizards in the semiarid/arid zone of Australia are reviewed to identify the influence of size (female mean snout-vent length), phylogeny (family effects) and ecological parameters on the evolution of life history traits of these species. Species producing more than one clutch per year are larger than single-clutched ones. In an ANCOVA, significant effects of size and phylogeny on clutch size and on age at sexual maturity were found. Microhabitat (arboreal, terrestrial, and subterranean life style) also had an effect on clutch size, but only mediated through a significant interaction with size. However, results of the ANCOVAs depend on the families and ecological parameters included in the analyses. Therefore, caution is necessary in interpreting or generalizing the results; in any case, size and phylogeny explain only a small percentage of the observed variation. Nevertheless, a direct comparison of a set of syntopic/paratopic desert lizards supports and extends the main conclusions of the ANCOVA. A significant but small phylogenetic effect was found, and arboreal microhabitat was associated with greater age at sexual maturity. Activity (diurnal versus nocturnal) influenced yearly mortalities and clutch frequencies. For both, microhabitat and activity, predation levels and size-dependent mortality were the likely selective factors causing these correlations. The demographic environment explains the paucity of duurnal lizard species with fixed clutch sizes in the semiarid/arid zone of Australia. Possible causes for the evolution of fixed clutch sizes are discussed.     

Demographic response of snake-necked turtles correlates with indigenous harvest and feral pig predation in tropical northern Australia

Species that mature late, experience high levels of survival and have long generation times are more vulnerable to chronic increases in mortality than species with higher fecundity and more rapid turnover of generations. Many chelonians have low hatchling survival, slow growth, delayed sexual maturity and high subadult and adult survival. This constrains their ability to respond quickly to increases in adult mortality from harvesting or habitat alteration. In contrast, the northern snake-necked turtle Chelodina rugosa (Ogilby 1890) is fast-growing, early maturing and highly fecund relative to other turtles, and may be resilient to increased mortality. Here we provide correlative evidence spanning six study sites and three field seasons, indicating that C. rugosa is able to compensate demographically to conditions of relatively low subadult and adult survival, caused by pig Sus scrofa (Linnaeus 1758) predation and customary harvesting by humans. Recruitment and age specific fecundity tended to be greater in sites with low adult and subadult survival (and thus reduced densities of large turtles), owing to higher juvenile survival, a smaller size at onset of maturity and faster post-maturity growth. These patterns are consistent with compensatory density-dependent responses, and as such challenge the generality that high subadult and adult survival is crucial for achieving long-term population stability in long-lived vertebrates such as chelonians. We posit that long-lived species with 'fast' recruitment and a capacity for a compensatory demographic response, similar to C. rugosa, may be able to persist in the face of occasional or sustained adult harvest without inevitably threatening population viability.     

RELATIONSHIPS BETWEEN GENETIC VARIABILITY AND LIFE-HISTORY FEATURES OF BONY FISHES

Correlations between genetic variation and life-history variables were obtained for 80 species of bony fishes as a means of testing the hypothesis that genetic variation is directly related to 1) opportunity for balancing selection, as indicated by fecundity, and 2) environmental variation, as indicated by capacity for population increase. Genetic data were taken from the literature, and data on longevity, age at maturity, egg size, body size, and lifetime fecundity were taken from the literature where available and were otherwise estimated from other variables. Average heterozygosity does not increase significantly with increasing fecundity. However, heterozygosity is significantly associated with short generation times, quick maturation, small maximum size, and small eggs. Thus, heterozygosity appears to increase on a demographic continuum toward maximum values in species that are most strongly selected for maximizing the intrinsic rate of increase. Such species are associated with less stable environments. Thus, the results indicate a predominate role for environmental variation in controlling genetic variation of bony fishes.     

Demographic response of plant populations to habitat fragmentation and temporal environmental variability

Many plant species currently exist in fragmented populations of different sizes, while they also experience unpredictable climatic fluctuation over time. However, we still understand little about how plant demography responds to such spatial and temporal environmental variability. We studied population dynamics of an understory perennial herb Trillium camschatcense in the Tokachi plain of Hokkaido, Japan, where a significant effect of forest fragmentation on seedling recruitment was previously reported. Four populations across a range of fragment sizes were studied for 6 years, and the data were analyzed using matrix population models. Per capita fecundity (the number of recruits per plant) varied greatly among populations, but the variation in population growth rates (λ) was mainly driven by the variation in stasis and growth rates, suggesting that the general trend of reduced fecundity in fragmented populations may not be readily translated into subsequent dynamics. Temporal variation in λ among years was more than 2 times larger than spatial variation among populations, and this result was likely attributable to the contrasting response of correlation structures among demographic rates. The among-population variation in λ was dampened by negative covariation between matrix elements possibly due to density-dependent regulation as well as an inherent constraint that some elements are not independent, whereas positive covariation between matrix elements resulted in large temporal variation in λ. Our results show that population dynamics responded differently to habitat fragmentation and temporal variability of the environment, emphasizing the need to discriminate these spatial and temporal variations in demographic models. Although no populations were projected to be declining in stochastic simulations, correlation between current habitat size and plant density implies historical λ is positively related to habitat size.     

Effect of resource gradient on age and size at maturity and their influence on early‐life fecundity in the predatory Asian lady beetle,Harmonia axyridis

Variation in food availability impacts the performance of insects in terms of their size and age to maturity and fecundity. Age at maturity determines how quickly individuals in a population can start to reproduce and how much they can reproduce. Results from studies on various insect species show that food availability influences the size and fecundity of adult females. It is predicted that under poor growth conditions, variation in size is low, but variation in age at maturity is considerable. This prediction was examined in a widely distributed lady beetle species, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), a predator of aphids and coccids. Using a food gradient from low to high aphid prey density, performance of females that were reared on excess food was recorded for pre‐reproductive duration, size at reproductive maturity, number of aphids consumed, and fecundity in the first 10 days of their reproductive period. Results suggested that female H. axyridis that were reared on surplus food when kept at low prey density (poor growth condition) took, on average, three times longer to attain maturity and produced, on average, 14 times fewer eggs than females that were also reared on surplus food, but kept at high prey density (good growth condition). Females performed best at a prey density of 30 aphids per female per 150 cm². Results suggested that the current food availability significantly influenced the age and size of females at maturity and their fecundity. Age and size at maturity of female lady beetles showed non‐linear responses to prey density as well as the occurrence of a minimum size of females, below which H. axyridis females fail to mature. The steep slope recorded at lower prey densities suggests relatively high variation in age at maturity but low variation in size.     

Body size variation among mainland populations of the western rattlesnake (Crotalus viridis)

In general, squamate reptiles follow the converse to Bergmann's rule, attaining smaller sizes in cooler environments, whereas other vertebrate groups follow Bergmann's rule, attaining larger sizes in cooler areas. Intensive studies of body size evolution for species of squamates are necessary to understand the processes responsible for this trend. Here I present data on body size variation among mainland populations of the western rattlesnake, Crotalus viridis. This species consists of two well-differentiated phylogenetic clades, therefore all analyses were performed for the C. viridis group as a whole and separately for each of the two clades within the C. viridis group. Although both phylogenetic and nonphylogenetic analyses were performed, the data did not show phylogenetic conservatism, and therefore the nonphylogenetic results are preferred. I found no significant relationships between mean adult female snout-vent length and any of the physical and climatic variables that were examined for the C. viridis group using simple linear regression analysis. Examined separately, I found that individuals of the western clade, C. oreganus, were smaller in cooler and more seasonal environments, whereas individuals of the eastern clade. C. viridis sensu stricto, were larger in cooler and more seasonal areas. Thus, the observed size trends were in opposite directions for the two clades. Multiple regression analysis revealed that seasonality was a stronger predictor of body size variation than was temperature for both clades. The differences in body size trends between these clades may be due to differences in mortality rates among populations.     

Retired flies,hidden plateaus,and the evolution of senescence in Drosophila melanogaster

Late‐life plateaus in age‐specific mortality have been an evolutionary and biodemographic puzzle for decades. Although classic theory on the evolution of senescence predicts late‐life walls of death, observations in experimental organisms document the opposite trend: a slowing in the rate of increase of mortality at advanced ages. Here, I analyze published life‐history data on individual Drosophila melanogaster females and argue for a fundamental change in our understanding of mortality in this important model system. Mortality plateaus are not, as widely assumed, exclusive to late life, and are not explained by population heterogeneity—they are intimately connected to individual fecundity. Female flies begin adult life in the working stage, a period of active oviposition and low but accelerating mortality. Later they transition to the retired stage, a terminal period characterized by limited fecundity and relatively constant mortality. Because ages of transition differ between flies, age‐synchronized cohorts contain a mix of working and retired flies. Early‐ and mid‐life plateaus are obscured by the presence of working flies, but can be detected when cohorts are stratified by retirement status. Stage‐specificity may be an important component of Drosophila life‐history evolution.     

The effect of differential reproductive success on population genetic structure: correlations of life history with matrilines in humpback whales of the gulf of maine

To examine whether demographic and life-history traits are correlated with genetic structure, we contrasted mtDNA lineages of individual humpback whales (Megaptera novaeangliae) with sighting and reproductive histories of female humpback whales between 1979 and 1995. Maternal lineage haplotypes were obtained for 323 whales, either from direct sequencing of the mtDNA control region (n = 159) or inferred from known relationships along matrilines from the sequenced sample of individuals (n = 164). Sequence variation in the 550 bp of the control region defined a total of 19 maternal lineage haplotypes that formed two main clades. Fecundity increased significantly over the study period among females of several lineages among the two clades. Individual maternal lineages and other clades were characterized by significant variation in fecundity. The detected heterogeneity of reproductive success has the potential to substantially affect the frequency and distribution of maternal lineages found in this population over time. There were significant yearly effects on adult resighting rates and calf survivorship based on examination of sighting histories with varying capture-recapture probability models. These results indicate that population structure can be influenced by interactions or associations between reproductive success, genetic structure, and environmental factors in a natural population of long-lived mammals.     

Evolutionary genetics of aging in Daphnia

Evolutionary theory of aging stipulates that aging is inevitable consequence of low effectiveness of natural selection acting on traits expressed late in the life span of the organisms. Two main hypotheses exist: the neutralist mutation-accumulation theory and selectionist antagonistic pleiotropy theory. Both theories predict the increase of genetic variance with age; the antagonistic pleiotropy theory also predicts negative genetic correlation between fitness related traits in the beginning and in the end of the life span. In order to test these predictions we measured life expectancy and age specific mortality in cohorts of 26 c lones of Daphnia magna extracted from a single cyclic parthenogen population. Simultaneously, fecundity and age to maturity were measured in representatives of the same clones. Log mortality increased linearly with age, with little evidence for leveling off, although some replicate cohorts did show a significant leveling off of mortality. Genetic variance of log mortality was significantly higher in the last quarter of the life span than in earlier time intervals. There was a significant positive genetic correlation between early fecundity and early mortality, but not between early fecundity and late mortality. This indicates that, although there is a trade-off between fecundity and survival, this trade-off is not based on pleiotropy across ages and therefore the data does not support the prediction of antagonistic pleiotropy theory.