Inevitable evolution: back to the origin and beyond the 20th century paradigm of contingent evolution by historical natural selection

Since neo-Darwinism arose from the work of Darwin and Mendel evolution by natural selection has been seen as contingent and historical being defined by an a posteriori selection process with no a priori laws that explain why evolution on Earth has taken the direction of the major evolutionary trends and transitions instead of any other direction. Recently, however, major life-history trends and transitions have been explained as inevitable because of a deterministic selection that unfolds from the energetic state of the organism and the density-dependent competitive interactions that arise from self-replication in limited environments. I describe differences and similarities between the historical and deterministic selection processes, illustrate concepts using life-history models on large body masses and limited reproductive rates, review life-history evolution with a wider focus on major evolutionary transitions, and propose that biotic evolution is driven by a universal natural selection where the long-term evolution of fitness-related traits is determined mainly by deterministic selection, while contingency is important predominately for neutral traits. Given suitable environmental conditions, it is shown that selection by energetic state and density-dependent competitive interactions unfolds to higher level selection for life-history transitions from simple asexually reproducing self-replicators to large bodied organisms with senescence and sexual reproduction between males and females, and in some cases, to the fully evolved eusocial colony with thousands of offspring workers. This defines an evolutionary arrow of time for open thermodynamic systems with a constant inflow of energy, predicting similar routes for long-term evolution on similar planets.     

Unexpected discontinuities in life-history evolution under size-dependent mortality

In many organisms survival depends on body size. We investigate the implications of size-selective mortality on life-history evolution by introducing and analysing a new and particularly flexible life-history model with the following key features: the lengths of growth and reproductive periods in successive reproductive cycles can vary evolutionarily, the model does not constrain evolution to patterns of either determinate or indeterminate growth, and lifetime number and sizes of broods are the outcomes of evolutionarily optimal life-history decisions. We find that small changes in environmental conditions can lead to abrupt transitions in optimal life histories when size-dependent mortality is sufficiently strong. Such discontinuous switching results from antagonistic selection pressures and occurs between strategies of early maturation with short reproductive periods and late maturation with long reproductive cycles. When mortality is size-selective and the size-independent component is not too high, selection favours prolonged juvenile growth, thereby allowing individuals to reach a mortality refuge at large body size before the onset of reproduction. When either component of mortality is then increased, the mortality refuge first becomes unattractive and eventually closes up altogether, resulting in short juvenile growth and frequent reproduction. Our results suggest a new mechanism for the evolution of life-history dimorphisms.     

Before senescence: the evolutionary demography of ontogenesis

The age-specific mortality curve for many species, including humans, is U-shaped: mortality declines with age in the developing cohort (ontogenescence) before increasing with age (senescence). The field of evolutionary demography has long focused on understanding the evolution of senescence while largely failing to address the evolution of ontogenescence. The current review is the first to gather the few available hypotheses addressing the evolution of ontogenescence, examine the basis and assumptions of each and ask what the phylogenetic extent of ontogenescence may be. Ontogenescence is among the most widespread of life-history traits, occurring in every population for which I have found sufficiently detailed data, in major groups throughout the eukaryotes, across many causes of death and many life-history types. Hypotheses seeking to explain ontogenescence include those based on kin selection, the acquisition of robustness, heterogeneous frailties and life-history optimization. I propose a further hypothesis, arguing that mortality drops with age because most transitions that could trigger the risks caused by genetic and developmental malfunctions are concentrated in early life. Of these hypotheses, only those that frame ontogenescence as an evolutionary by-product rather than an adaptation can explain the tremendous diversity of organisms and environments in which it occurs.     

Does encephalization correlate with life history or metabolic rate in Carnivora?

A recent analysis of brain size evolution reconstructed the plesiomorphic brain–body size allometry for the mammalian order Carnivora, providing an important reference frame for comparative analyses of encephalization (brain volume scaled to body mass). I performed phylogenetically corrected regressions to remove the effects of body mass, calculating correlations between residual values of encephalization with basal metabolic rate (BMR) and six life-history variables (gestation time, neonatal mass, weaning time, weaning mass, litter size, litters per year). No significant correlations were recovered between encephalization and any life-history variable or BMR, arguing against hypotheses relating encephalization to maternal energetic investment. However, after correcting for clade-specific adaptations, I recovered significant correlations for several variables, and further analysis revealed a conserved carnivoran reproductive strategy, linking degree of encephalization to the well-documented mammalian life-history trade-off between neonatal mass and litter size. This strategy of fewer, larger offspring correlating with increased encephalization remains intact even after independent changes in encephalization allometries in the evolutionary history of this clade.     

Lifetime reproductive effort

In a 1966 American Naturalist article, G. C. Williams initiated the study of reproductive effort (RE) with the prediction that longer-lived organisms ought to expend less in reproduction per unit of time. We can multiply RE, often measured in fractions of adult body mass committed to reproduction per unit time, by the average adult life span to get lifetime reproductive effort (LRE). Williams's hypothesis (across species, RE decreases as life span increases) can then be refined to read "LRE will be approximately constant for similar organisms." Here we show that LRE is a key component of fitness in nongrowing populations, and thus its value is central to understanding life-history evolution. We then develop metabolic life-history theory to predict that LRE ought to be approximately 1.4 across organisms despite extreme differences in production and growth rates. We estimate LRE for mammals and lizards that differ in growth and production by five- to tenfold. The distributions are approximately normal with means of 1.43 and 1.41 for lizards and mammals, respectively (95% confidence intervals: 1.3-1.5 and 1.2-1.6). Ultimately, therefore, a female can only produce a mass of offspring approximately equal to 1.4 times her own body mass during the course of her life.     

NATURAL SELECTION REDUCES ENERGY METABOLISM IN THE GARDEN SNAIL, HELIX ASPERSA (CORNU ASPERSUM)

Phenotypic selection is widely recognized as the primary cause of adaptive evolution in natural populations, a fact that has been documented frequently over the last few decades, mainly in morphological and life-history traits. The energetic definition of fitness predicts that natural selection will maximize the residual energy available for growth and reproduction, suggesting that energy metabolism could be a target of selection. To address this problem, we chose the garden snail, Helix aspersa ( Cornu aspersum ). We performed a seminatural experiment for measuring phenotypic selection on standard metabolic rate (SMR), the minimum cost of maintenance in ectotherm organisms. To discount selection on correlated traits, we included two additional whole-organism performance traits (mean speed and maximum force of dislodgement). We found a combination of linear (negative directional selection, β=−0.106 ± 0.06; P = 0.001) and quadratic (stabilizing selection, γ=−0.012 ± 0.033; P = 0.061) selection on SMR. Correlational selection was not significant for any possible pair of traits. This suggests that individuals with average-to-reduced SMRs were promoted by selection. To the best of our knowledge, this is the first study showing significant directional selection on the obligatory cost of maintenance in an animal, providing support for the energetic definition of fitness.     

Environmental complexity,life history,and encephalisation in human evolution

Brain size has increased threefold during the course of human evolution, whilst body weight has approximately doubled. These increases in brain and body size suggest that reproductive (and, therefore, evolutionary) rates must have slowed considerably during this period. During the same period, however, environmental heterogeneity has increased substantially. A central tenet of life-history theory states that in heterogeneous environments, organisms with fast life histories will be favoured. The human lineage, therefore, has proceeded in direct contradiction of this theory. This contribution attempts to resolve this contradiction by recourse to Godfrey-Smith’s Environmental Complexity Thesis, which states that the function of cognition is to enable the organism to deal with environmental complexity. It is suggested that among slowly reproducing organisms the behavioural flexibility provided by advanced cognitive abilities is a fundamental component of adaptation to heterogeneous environments. In the human lineage this flexibility is manifest particularly in the increasing complexity of material culture.     

Revising the distributive networks models of West, Brown and Enquist (1997) and Banavar, Maritan and Rinaldo (1999): metabolic inequity of living tissues provides clues for the observed allometric scaling rules

Basic assumptions of two distributive network models designed to explain the 3/4 power scaling between metabolic rate and body mass are re-analysed. It is shown that these models could have consistently accounted for the observed scaling patterns if and only if body mass M had scaled as L4, where L is body length, in the model of Banavar et al. (1999, Nature 399, 130-132), or if spatial volume VF occupied by the distributive network had scaled as M3/4 in the model of West et al. (1997, Science 276, 122-126). Lack of agreement between these predictions and observational evidence invalidates both models rendering them mathematically controversial. It is further shown that consideration of distributive networks can nevertheless yield realistic values of scaling exponents under the major assumption that living organisms are designed so as to keep the mass-specific metabolic rate of important functional tissues in the vicinity of a size-independent optimum value. Mass-specific metabolic rate of subsidiary mechanical tissues can be small and vary with body mass. Different patterns of spatial distribution of metabolically active biomass within the organism result in different patterns of allometric scaling. From the available evidence the presumable optimum value of mass-specific metabolic rate of living matter is estimated to be in the vicinity of 1-10 W kg-1.     

Time and energy constraints in pinniped lactation

Previous reviews have recognized patterns of lactation in pinnipeds divided along phylogenetic lines. This study extended previous models of lactation in pinnipeds by explicitly taking into account all the energetic costs to mothers. Based on an analysis of time-energy budgets, the feasible lactation strategy for a species can be shown to depend on body mass. Due to increased metabolic costs of maintenance, species with a large body mass cannot normally sustain lactation by foraging during lactation unless they have access to rich local prey resources. Consequently, large pinnipeds must normally sustain lactation from body reserves. This disadvantage is compensated in large pinnipeds by freedom to forage in support of offspring at greater range whereas small pinnipeds are restricted to foraging within the locality of the pupping colony. In the absence of correlations between major life-history variables and body mass in pinnipeds, the principal patterns of lactation are likely to be different solutions to the trade-off between foraging on a relatively rich prey resource at long range and foraging on a poorer prey resource within a restricted range. Hence phylogeny may be less important than adaptation in the evolution of pinniped lactation.     

Effects of body size and temperature on population growth

For at least 200 years, since the time of Malthus, population growth has been recognized as providing a critical link between the performance of individual organisms and the ecology and evolution of species. We present a theory that shows how the intrinsic rate of exponential population growth, rmax, and the carrying capacity, K, depend on individual metabolic rate and resource supply rate. To do this, we construct equations for the metabolic rates of entire populations by summing over individuals, and then we combine these population-level equations with Malthusian growth. Thus, the theory makes explicit the relationship between rates of resource supply in the environment and rates of production of new biomass and individuals. These individual-level and population-level processes are inextricably linked because metabolism sets both the demand for environmental resources and the resource allocation to survival, growth, and reproduction. We use the theory to make explicit how and why rmax exhibits its characteristic dependence on body size and temperature. Data for aerobic eukaryotes, including algae, protists, insects, zooplankton, fishes, and mammals, support these predicted scalings for rmax. The metabolic flux of energy and materials also dictates that the carrying capacity or equilibrium density of populations should decrease with increasing body size and increasing temperature. Finally, we argue that body mass and body temperature, through their effects on metabolic rate, can explain most of the variation in fecundity and mortality rates. Data for marine fishes in the field support these predictions for instantaneous rates of mortality. This theory links the rates of metabolism and resource use of individuals to life-history attributes and population dynamics for a broad assortment of organisms, from unicellular organisms to mammals.     

Immune challenge affects basal metabolic activity in wintering great tits

The costs of exploiting an organism's immune function are expected to form the basis of many life-history trade-offs. However, there has been debate about whether such costs can be paid in energetic and nutritional terms. We addressed this question in a study of wintering, free-living, male great tits by injecting them with a novel, non-pathogenic antigen (sheep red blood cells) and measuring the changes in their basal metabolic rates and various condition indices subsequent to immune challenge. The experiment showed that activation of the immune system altered the metabolic activity and profile of immune cells in birds during the week subsequent to antigen injection: individuals mounting an immune response had nearly 9% higher basal metabolic rates, 8% lower plasma albumin levels and 37% higher heterophile-to-lymphocyte ratios (leucocytic stress indices) than sham-injected control birds. They also lost nearly 3% (0.5 g) of their body mass subsequent to the immune challenge. Individuals that mounted stronger antibody responses lost more mass during the immune challenge. These results suggest that energetic expenditures to immune response may have a non-trivial impact upon an individual's condition.     

Predicting the response to simultaneous selection: genetic architecture and physiological constraints

A great deal is known about the evolutionary significance of body size and development time. They are determined by the nonlinear interaction of three physiological traits: two hormonal events and growth rate (GR). In this study we investigate how the genetic architecture of the underlying three physiological traits affects the simultaneous response to selection on the two life-history traits in the hawkmoth Manduca sexta. The genetic architecture suggests that when the two life-history traits are both selected in the same direction (to increase or decrease) the response to selection is primarily determined by the hormonal mechanism. When the life-history traits are selected in opposite directions (one to increase and one to decrease) the response to selection is primarily determined by factors that affect the GR. To determine how the physiological traits affect the response to selection of the life-history traits, we simulated the predicted response to 10 generations of selection. A total of 83% of our predictions were supported by the simulation. The main components of this physiological framework also exist in unicellular organisms, vertebrates, and plants and can thus provide a robust framework for understanding how underlying physiology can determine the simultaneous evolution of life-history traits.     

Energetics and life-history of bats in comparison to small mammals

Mammals can be aligned along a slow-fast life-history continuum and a low–high metabolic rate continuum based on their traits. Small non-volant mammals occupy the fast/high end in both continua with high reproductive rates and short life spans linked with high mass-specific metabolic rates. Bats occupy the high end of the metabolic continuum, but the slow end of the life-history continuum with low reproductive rates and long life spans. Typically, both continua are linked, and similar life-history traits of species are reflected in more similar metabolic rates. We therefore hypothesized that metabolic rates are similar in species with similar life-history traits. Resting metabolic rates (RMR) were measured for three ecologically and morphologically similar sympatric bat species (Myotis nattereri, M. bechsteinii, and Plecotus auritus; Vespertilionidae) and compared to data from other similar-sized, temperate insectivorous mammals with other life-history strategies. The bat species share similar life-histories and RMRs, both of which differ from the remaining mammals and therefore supporting our hypothesis. To verify that bats are similar in RMR, two energetically contrasting periods were compared. RMRs in post-lactating females did not differ between bat species. It was, however, positively correlated with parasite load in both Myotis species. However, RMRs differed during energy-demanding pregnancy where M. nattereri had the significantly lowest RMR, suggesting metabolic compensation as an energy-saving strategy. We conclude that the energy requirements of bat species with similar life-history traits resemble each other during periods of low energetic demands and are more similar to each other than to other small temperate mammals.     

Insulin-like growth factor-1 is associated with life-history variation across Mammalia

Despite the diversity of mammalian life histories, persistent patterns of covariation have been identified, such as the ‘fast–slow’ axis of life-history covariation. Smaller species generally exhibit ‘faster’ life histories, developing and reproducing rapidly, but dying young. Hormonal mechanisms with pleiotropic effects may mediate such broad patterns of life-history variation. Insulin-like growth factor 1 (IGF-1) is one such mechanism because heightened IGF-1 activity is related to traits associated with faster life histories, such as increased growth and reproduction, but decreased lifespan. Using comparative methods, we show that among 41 mammalian species, increased plasma IGF-1 concentrations are associated with fast life histories and altricial reproductive patterns. Interspecific path analyses show that the effects of IGF-1 on these broad patterns of life-history variation are through its direct effects on some individual life-history traits (adult body size, growth rate, basal metabolic rate) and through its indirect effects on the remaining life-history traits. Our results suggest that the role of IGF-1 as a mechanism mediating life-history variation is conserved over the evolutionary time period defining mammalian diversification, that hormone–trait linkages can evolve as a unit, and that suites of life-history traits could be adjusted in response to selection through changes in plasma IGF-1.     

Ageing and immortality

The concept of the force of natural selection was developed to explain the evolution of ageing. After ageing, however, comes a period in which mortality rates plateau and some individual organisms could, in theory, live forever. This late-life immortality has no presently agreed upon explanation. Two main theories have been offered. The first is heterogeneity within ageing cohorts, such that only extremely robust individuals survive ageing. This theory can be tested by comparisons of more and less robust cohorts. It can also be tested by fitting survival data to its models. The second theory is that late-life plateaus in mortality reflect the inevitable late-life plateau in the force of natural selection. This theory can be tested by changing the force of natural selection in evolving laboratory populations, particularly the age at which the force plateaus. This area of research has great potential for elucidating the overall structure of life-history evolution, particularly the interrelationship between the three life-history phases of development, ageing and immortality.     

Stage-structured cycles generate strong fitness-equalizing mechanisms

For many organisms, rates of reproduction, growth and mortality depend on the amount of resources that an individual consumes. When resource abundances fluctuate through space and time, the realized life-history of an individual can change dramatically depending on the dynamics experienced. Previous studies have investigated the influence of resource-dependent rates on population dynamics, but none have considered how the feedback between non-equilibrium resource dynamics and resource-dependent life-histories influence natural selection and the maintenance of genetic diversity within populations. Here we demonstrate that different patterns of resource dynamics have a strong impact on natural selection in organisms with resource-dependent life-histories. Small-amplitude consumer-resource cycles, lead to lower rates of natural selection than do large-amplitude consumer-resource cycles. Parameterizing the model for a Daphnia-algal system, we demonstrate that resource-dependent life-history can explain the recently published observation that selection among Daphnia genotypes changed depending on the pattern of algal resource fluctuations. The characteristically asexual reproduction of Daphnia allows us to draw a much-needed link to the large body of competition theory that has emerged from community ecology. Our results reveal that the common ecological features of resource-dependent life-history and ontogenetic size-structure generate strong fitness equalizing mechanisms that likely contribute to the maintenance of diversity in natural systems. Electronic Supplementary Material Supplementary material is available in the online version of this article at accessible for authorized users.     

Ecological and evolutionary physiology of desert birds: a progress report

The adaptive significance of mechanisms of energy and water conservation among species of desert rodents, which avoid temperature extremes by remaining within a burrow during the day, is well established. Conventional wisdom holds that arid-zone birds, diurnal organisms that endure the brunt of their environment, occupy these desert climates because of the possession of physiological design features common to all within the class Aves. We review studies that show that desert birds may have evolved specific features to deal with hot desert conditions including: a reduced basal metabolic rate (BMR) and field metabolic rate (FMR), and lower total evaporative water loss (TEWL) and water turnover (WTO).Previous work on the comparative physiology of desert birds relied primarily on information gathered on species from the deserts of the southwestern U.S., which are semi-arid habitats of recent geologic origin. We include data on species from Old World deserts, which are geologically older than those in the New World, and place physiological responses along an aridity axis that includes mesic, semi-arid, arid, and hyperarid environments.The physiological differences between desert and mesic birds that we have identified using the comparative method could arise as a result of acclimation to different environments, of genetic change mediated by selection, or both. We present data on the flexibility of BMR and TEWL in Hoopoe Larks that suggest that phenotypic adjustments in these variables can be substantial. Finally, we suggest that linkages between the physiology of individual organism and its life-history are fundamental to the understanding of life-history evolution.     

A new view of avian life-history evolution tested on an incubation paradox

Viewing life-history evolution in birds based on an age-specific mortality framework can explain broad life-history patterns, including the long incubation periods in southern latitudes documented here. I show that incubation periods of species that are matched phylogenetically and ecologically between Argentina and Arizona are longer in Argentina. Long incubation periods have mystified scientists because they increase the accumulated risk of time-dependent mortality to young without providing a clear benefit. I hypothesize that parents of species with low adult mortality accept increased risk of mortality to their young from longer incubation if this allows reduced risk of mortality to themselves. During incubation, songbird parents can reduce risk of mortality to themselves by reducing nest attentiveness (percentage of time on the nest). Here I show that parents of species with lower adult mortality exhibit reduced nest attentiveness and that lower attentiveness is associated with longer incubation periods. However, the incubation period is also modified by juvenile mortality. Clutch size variation is also strongly correlated with age-specific mortality. Ultimately, adult and juvenile mortality explain variation in incubation and other life-history traits better than the historical paradigm.     

GENETIC CORRELATIONS BETWEEN LIFE-HISTORY AND BEHAVIORAL TRAITS CAN CAUSE REPRODUCTIVE ISOLATION

Reproductive isolation may often evolve as an indirect (pleiotropic) consequence of populations adapting to different environments or habitats. For example, niches that are temporally or seasonally offset can select for organisms with different developmental characteristics. These developmental differences can inadvertently cause reproductive isolation by a variety of means including shifts in mating activity patterns. Here, we show a genetic correlation between a life-history trait (developmental period) and a behavioral trait (time of mating) that causes significant premating isolation in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Fly lines selected for short and long developmental periods differ in their preferred times of mating during the evening. This difference translates into significant prezygotic isolation, as measured by mate choice tests. If the time of mating between two populations differed more than one hour, the isolation index was significantly higher than zero. These indicate that premating isolation can be established if the developmental period is divergently selected for. If such genetic correlations are ubiquitous in many organisms, multifarious divergent selection for life-history traits would often accelerate the evolution of reproductive isolation. We speculate that reproductive isolation may have been evolved via genetic correlations among time-related traits, for example, developmental period and time of mating, as in other organisms.     

Evolution of the individual

This article studies the transition in evolution from single cells to multicellular organisms as a case study in the origin of individuality. The issues considered are applicable to all major transitions in the units of selection that involve the emergence of cooperation and the regulation of conflict. Explicit genetic models of mutation and selection both within and between organisms are studied. Cooperation among cells increases when the fitness covariance at the level of the organism overcomes within-organism change toward defection. Selection and mutation during development generate significant levels of within-organism variation and lead to variation in organism fitness at equilibrium. This variation selects for gem-line modifiers and other mediators of within-organism conflict, increasing the heritability of fitness at the organism level. The evolution of these modifiers is the first new function at the emerging organism level and a necessary component of the evolution of individuality.