Evolutionary walks through a land plant morphospace

A model for mimicking land plant evolution is here expanded and re-evaluated. The model consists of (1) a morphospace containing on the order of 10⁹ phenotypic variants, (2) 15 different fitness landscapes, each defined on the basis of performing one or more of four tasks (i.e. maximizing light interception, mechanical stability and reproduction, and minimizing total surface area), and (3) an algorithm driving a search through fitness landscapes for more fit variants. The model is used to predict the effects of the number of simultaneously performed tasks ('complexity'), abrupt changes in environmental conditions (mimicked by random replacement of one fitness landscape with another), and developmental barriers (mimicked by barring searches from entering specific subdomains in the morphospace) on number and accessibility of variants occupying fitness maxima. The model predicts that (1) the number and accessibility of fitness peaks will increase (while the difference between the relative fitness of peaks and valleys will decrease) in proportion to functional complexity, (2) abrupt shifts in landscapes will increase rather than decrease phenotypic diversity, and (3) obstructed searches have an equal or higher probability of reaching fitness peaks than unfettered searches. These results follow axiomatically from the way hypothetical variants are spatially ordered in the morphospace, the manner in which relative fitness is defined, and the protocol used to locate fitness peaks. A critique of the model's predictions and desiderata for future research are provided.     

Simulation of local evolutionary dynamics of small populations

A simple stochastic model assuming continuous traits, normally distributed modifications, selection for fertility and multiplicative fitness was used to simulate phenotypic evolution by reproducing individuals in a given fitness landscape. Of particular interest was how small populations cross saddles separating distinct adaptive peaks. The simulated evolution exhibits a strong dualism: at the same level of reproductive errors, sexual reproduction provides significantly better local adaptation and asexual repreduction provides significantly better adaptive dynamics.     

Phenotypic gender in Hormathophylla spinosa (Brassicaceae), a perfect hermaphrodite with tetradynamous flowers, is variable

Angiosperms show an evolutionary trend from an indefinite to a fixed number of floral organs. When floral formula inconstancy in recent angiosperms is reported, it is often considered as a byproduct of stress and its fitness consequences remain mostly unexplored. We report substantial nonhomeotic meristic variation in stamen number (0–10 stamens per flower) in two populations of Hormathophylla spinosa during four years. This variation was plastic, suggesting its functional role in the adjustment of phenotypic gender. However, no correlations were found between phenotypic gender and plant size, pollinator or herbivore abundance. Effects on female reproductive success were inconsistent on a per-flower and on a per-plant basis, rendering adaptive explanations in terms of selfing or resource adjustment unsatisfactory with the data available. Nevertheless, individuals showing larger interannual variation in phenotypic gender showed higher female reproductive success, suggesting an advantage for gender modification. Although our results do not easily conform to any adaptive explanation, this remarkable example of breakdown of trait canalization should stimulate the study of the mechanisms and ultimate causes responsible for the maintenance of fixed floral traits.     

Phenotypic engineering: using hormones to explore the mechanistic and functional bases of phenotypic variation in nature

Perhaps the best way to determine whether and how traits of organisms are currently adaptive is to alter them experimentally and compare the relative fitness of altered and unaltered individuals. We call this method phenotypic engineering. To the extent that natural selection moulds organisms on a trait-by-trait basis, we would expect fitness of unmanipulated (control) individuals to be higher than that of experimentally altered individuals. However, other outcomes are possible and of interest. If, for example, a single trait were altered and the fitness of manipulated and unmanipulated organisms were found to be similar, we might conclude that selection is not currently operating on the altered trait. Phenotypic engineering with hormones describes an experimental approach to the study of adaptive variation in suites of traits that are hormonally mediated and correlated in their expression. A likely outcome of such manipulations is that some traits would be altered so as to elevate fitness but that changes in other, correlated traits would lower fitness. If the net effect were to depress fitness, a process by which natural selection shapes and maintains organisms as integrated units would be demonstrated. We have employed this approach in studies of the Dark-eyed Junco Junco hyemalis, a small passerine whose reproductive success varies with the abundance of nest predators. We treated males with testosterone, documented the phenotypic consequences and related these to various measures of fitness. Summarizing results to date: Behavioural comparison of males treated with testosterone (T-males) and control males (C-males) shows that T-males sing more frequently, are less attentive to offspring, have larger home ranges and are more attractive to females. Physiologically, testosterone accelerates entry into breeding condition in spring (loss of winter lipid stores) and results in higher levels of corticosterone. If exposure to testosterone is prolonged beyond the breeding season, pre-basic moult is delayed or prevented. We are currently comparing T- and C-males with respect to corticosteroid binding proteins, sperm reserves, response to nestling vocalizations and neuroanatomy. The relationship between testosterone-induced phenotypic variation and fitness is still under study. When treatment extends well beyond the breeding season, testosterone significantly reduces survivorship; otherwise it does not. With respect to apparent reproductive success (i.e. estimates of paternity that are not based on genetic analysis), more young leave the nests of C-males than of T-males, but treatment groups do not differ in the number of young that reach independence. Preliminary data on realized reproductive success (i.e. number of genetic offspring sired) suggest that production as the result of extra-pair fertilizations is greater in T- than in C-males but that T-males lose paternity of more of the offspring of their social mates to other males. Continued investigation will, we hope, reveal the factors governing the trade-offs between male mating effort and parental effort and between survival and current reproduction, as well as the frequency with which the typical phenotype outperforms one that has been experimentally altered.     

The length of adaptive walks is insensitive to starting fitness in Aspergillus nidulans

Adaptation involves the successive substitution of beneficial mutations by selection, a process known as an adaptive walk. Gradualist models of adaptation, which assume that all mutations are small relative to the distance to a fitness optimum, predict that adaptive walks should be longer when the founding genotype is less well adapted. More recent work modeling adaptation as a sequence of moves in phenotype or genotype space predicts, by contrast, much shorter adaptive walks irrespective of the fitness of the founding genotype. Here, we provide what is, to the best of our knowledge, the first direct test of these alternative models, measuring the length of adaptive walks in evolving lineages of fungus that differ initially in fitness. Contrary to the gradualist view, we show that the length of adaptive walks in the fungus Aspergillus nidulans is insensitive to starting fitness and involves just two mutations on average. This arises because poorly adapted populations tend to fix mutations of larger average effect than those of better-adapted populations. Our results suggest that the length of adaptive walks may be independent of the fitness of the founding genotype and, moreover, that poorly adapted populations can quickly adapt to novel environments.     

Wealth, status, and fitness: a historical study of Norwegians in variable environments

Wealth and status covary with lifetime reproductive success in preindustrial human populations. Local ecology is likely to modify this association, but details of this presumed relationship are not yet known. We sought to determine whether local ecology modifies the relationship between status and fitness (number of grandchildren). Our approach to the problem was to measure variation in fitness relative to status (landless or with land) and to local ecology (inland versus coastal communities). We also analyzed life history traits that might explain observed variations in fitness. Our results confirm previous findings that both status (landless=9.9 vs. with land=16.5) and ecology (inland=12.3 vs. coast=14.1) affect the number of grandchildren produced by a female in pre-industrial society. We also found that the differences in number of children between the status groups were less pronounced on the coast (landless=12.0 vs. with land=16.1) than inland (landless=7.8 vs. with land=16.8). Our findings are novel because they suggest that the fitness consequences of human status may depend on details of local ecology. We discuss four different mechanisms that could account for these fitness differences: (1) differential reproductive rate of mothers, (2) differential marriage rate of children (3) differential survival rate of children, and (4) different social practices (breastfeeding, inheritance of property and diet).     

HIGHER FITNESS FOR PHILOPATRIC THAN FOR IMMIGRANT MALES IN A SEMI-ISOLATED POPULATION OF GREAT REED WARBLERS

To compare the fitness of philopatric and immigrant individuals we examined the lifetime reproductive success of 116 male and 137 female great reed warblers. The study was carried out in a semi-isolated population in Sweden and covered breeding adults hatched between 1985 and 1993. Lifetime fitness, measured as life time number of fledglings and offspring recruits, was lower for immigrant than for philopatric males. We found no such relationships for females. The difference in reproductive success could not be explained by immigrant males having lower phenotypic quality because they had similar life span, spring arrival date, and territory quality as philopatric males. The lower lifetime fitness among immigrant than philopatric males appeared to result from reduced mating success. This suggests that females are reluctant to mate with immigrant males despite their apparently similar phenotypic quality. Though it is not known whether females gain in fitness by avoiding matings with immigrant males, it is notable that immigrant males have smaller song repertoires than philopatric males. Large repertoires, previously shown to sexually arouse great reed warbler females, correlate with the occurrence of extrapair paternity and postfledging survival of offspring in our population.     

Rampant False Detection of Adaptive Phenotypic Optimization by ParTI-Based Pareto Front Inference

Organisms face tradeoffs in performing multiple tasks. Identifying the optimal phenotypes maximizing the organismal fitness (or Pareto front) and inferring the relevant tasks allow testing phenotypic adaptations and help delineate evolutionary constraints, tradeoffs, and critical fitness components, so are of broad interest. It has been proposed that Pareto fronts can be identified from high-dimensional phenotypic data, including molecular phenotypes such as gene expression levels, by fitting polytopes (lines, triangles, tetrahedrons, and so on), and a program named ParTI was recently introduced for this purpose. ParTI has identified Pareto fronts and inferred phenotypes best for individual tasks (or archetypes) from numerous data sets such as the beak morphologies of Darwin’s finches and mRNA concentrations in human tumors, implying evolutionary optimizations of the involved traits. Nevertheless, the reliabilities of these findings are unknown. Using real and simulated data that lack evolutionary optimization, we here report extremely high false-positive rates of ParTI. The errors arise from phylogenetic relationships or population structures of the organisms analyzed and the flexibility of data analysis in ParTI that is equivalent to p-hacking. Because these problems are virtually universal, our findings cast doubt on almost all ParTI-based results and suggest that reliably identifying Pareto fronts and archetypes from high-dimensional phenotypic data are currently generally difficult.     

Lifetime offspring production in relation to breeding lifespan, attractiveness, and mating status in male collared flycatchers

As a comprehensive fitness parameter, lifetime reproductive success (LRS) is influenced by many different environmental and genetic factors, among which longevity is one of the most important. These factors can be reflected in secondary sexual characters, which may affect the life histories of individuals via social relations with conspecifics. Facultative polygyny in birds is another conspicuous reproductive trait that potentially increases male reproductive success, but lifetime success data in relation to polygyny are scarce. Here, we used 17?years of breeding data to quantify the LRS of male collared flycatchers (Ficedula albicollis) on the basis of lifetime recruitment of offspring. Breeding lifespan showed a positive relationship with LRS, and it was also significantly associated with mean recruitment of offspring per breeding year. Body size and sexually selected forehead patch size did not predict the number of recruits. Polygyny was positively associated with LRS, but when we corrected for lifespan, this relationship disappeared. Our results demonstrate that the relationship between longevity and LRS is not explained by the higher number of reproductive attempts when living longer, and question the adaptive value of polygyny in this population. The lack of association between forehead patch size and recruitment suggests that forehead patch is a poor indicator of phenotypic quality in our birds.     

What determines the growth of individual castes in social trematodes?

Phenotypic diversification among colony members often leads to formation of physical castes which are morphologically specialised for particular tasks within the colony. The relative abundance of these castes and their body sizes represent two key aspects of the demography of a colony that may reflect the colony’s needs and conditions, and ultimately influence its survival and reproductive success. In a recently discovered social trematode, Philophthalmus sp., which exhibits a reproductive division of labour, the role of competition and colony composition in shaping reproductive success and behaviour of colony members has been documented. As body size variation within physical castes often influences colony efficiency, we investigated how the growth of reproductive and non-reproductive morphs of Philophthalmus sp. responds to competitive pressure, and to other attributes of colony demography such as colony size and composition. Our survey of a natural population and in vitro experiments demonstrate that the growth of reproductive colony members reflects the interaction between colony composition and the presence of a competitor, while the non-reproductive members simply grow larger in the presence of the intra-host competitor, Maritrema novaezealandensis. Furthermore, the close association between the volume and reproductive capacity of the reproductive members corroborates an adaptive value of colony member size in determining the fitness of the trematode colony as a whole. The present study is the first to demonstrate a fitness consequence, and identify the determinants, of the growth of colony members in social trematodes.     

Fitness of indirectly transmitted pathogens: restraint and constraint

Many pathogens of medical and veterinary importance have obligatory multihost life cycles. Yet, theoretical models aiming to predict patterns of pathogen reproductive success and the limited empirical data available with which to evaluate them, focus on directly transmitted microparasites. Patterns of host exploitation and the relative fitness of individual pathogen genotypes throughout the different host stages of multihost life cycles have thus remained ignored. We examined correlated responses to artificial selection of Schistosoma mansoni lines selected for high or low infection intensity in the intermediate host. Pathogen fitness in the intermediate host was strongly inversely correlated with pathogen fitness in the definitive host. Moreover, high pathogen infection intensity was associated with decreased, rather than increased, virulence to its intermediate host. These results raise important implications regarding the impact of genetic constraints on the maintenance of genetic and phenotypic polymorphisms in natural populations, the evolution and coevolution of parasite virulence and host specialization, as well as the success of host-directed control programs.     

Fitness effects of floral plasticity and thermoregulation in a thermally changing environment

Abstract To better understand the evolution of phenotypic plasticity and thermoregulation and their potential value for ectotherms in the face of global warming, we conducted field experiments to measure their effects on fitness and their association with reproductive phenology in Plantago lanceolata in a thermally variable environment. We measured the reproductive timing and success of genotypes varying in thermoregulation, as mediated by floral-reflectance plasticity. Results were consistent with the hypothesis that thermoregulation is more adaptive when thermally variable reproductive seasons are shorter and cooler. Strong thermoregulation/plasticity increased reproductive success during the cool portion of the reproductive season but not during the warm portion. Directional selection that favored strongly thermoregulating genotypes early in the season shifted to stabilizing selection that favored genotypes with weaker thermoregulation later in the season. Thermoregulation and reproductive phenology were negatively correlated. Although reproductive onset and duration were similar between genotypes, strong thermoregulators produced more and larger spikes (clutches) early; weak thermoregulators produced more spikes late. Results suggest that with atmospheric warming, the benefit of raising body temperature via thermoregulation when it is cool should decline in extant populations. The negative correlation between thermoregulation and phenology should accelerate the evolutionary shift toward thermoconformity, that is, reduced plasticity.     

Early determinants of lifetime reproductive success differ between the sexes in red deer.

In polygynous, sexually dimorphic species, sexual selection should be stronger in males than in females. Although this prediction extends to the effects of early development on fitness, few studies have documented early determinants of lifetime reproductive success in a natural mammal population. In this paper, we describe factors affecting the reproductive success of male and female red deer (Cervus elaphus) on the island of Rum, Scotland. Birthweight was a significant determinant of total lifetime reproductive success in males, with heavier-born males being more successful than lighter ones. In contrast, birthweight did not affect female reproductive success. High population density and cold spring temperatures in the year of birth decreased several components of fitness in females, but did not affect the breeding success of males. The results confirm the prediction that selection on a sexually dimorphic trait should be greater in males than in females, and explain the differential maternal expenditure between sons and daughters observed in red deer. Differences between the sexes in the effects of environmental and phenotypic variation on fitness may generate differences in the amount of heritable genetic variation underlying traits such as birthweight.     

Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra‐pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within‐pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra‐pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade‐off between male within‐pair paternity success and extra‐pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.     

Voice and handgrip strength predict reproductive success in a group of indigenous african females

Evolutionary accounts of human traits are often based on proxies for genetic fitness (e.g., number of sex partners, facial attractiveness). Instead of using proxies, actual differences in reproductive success is a more direct measure of Darwinian fitness. Certain voice acoustics such as fundamental frequency and measures of health such as handgrip strength correlate with proxies of fitness, yet there are few studies showing the relation of these traits to reproduction. Here, we explore whether the fundamental frequency of the voice and handgrip strength account for differences in actual reproduction among a population of natural fertility humans. Our results show that both fundamental frequency and handgrip strength predict several measures of reproductive success among a group of indigenous Namibian females, particularly amongst the elderly, with weight also predicting reproductive outcomes among males. These findings demonstrate that both hormonally regulated and phenotypic quality markers can be used as measures of Darwinian fitness among humans living under conditions that resemble the evolutionary environment of Homo sapiens. We also argue that these findings provide support for the Grandmother Hypothesis.     

SPERM COMPETITIVE ABILITY AND INDICES OF LIFETIME REPRODUCTIVE SUCCESS

Understanding the selection pressures shaping components of male reproductive success is essential for assessing the role of sexual selection on phenotypic evolution. A male's competitive reproductive success is often measured in sequential mating tests by recording P1 (first mating male) and P2 (second mating male) paternity scores. How each of these scores relates to a male's overall fitness, for example, lifetime reproductive success is, however, not known. This information is needed to determine whether males benefit from maximizing both P1 and P2 or by trading off P1 against P2 ability. We measured P1, P2, and an index of lifetime reproductive success (LRS_i, a male's competitive reproductive success measured over 12 days) for individual male Drosophila melanogaster. We found no evidence for phenotypic correlations between P1 and P2. In addition, whereas both P1 and P2 were associated with relative LRS_i, only P2 predicted absolute LRS_i. The results suggest that P2 was most closely linked to LRS_i in the wild‐type population studied, a finding which may be common to species with strong second male sperm precedence. The study illustrates how P1 and P2 can have differing relationships with a male's overall reproductive success, and highlights the importance of understanding commonly used measures of sperm competition in the currency of fitness.     

Natural selection on age-specific fertilities in human females: comparison of individual-level fitness measures.

Lifetime reproductive success and timing of reproduction are key components of life-history evolution. To understand the evolution of reproductive schedules, it is important to use a measure of fitness that is sensitive both to reproductive quantity and reproductive timing. There is a contradiction between the theory, which mainly focuses on the rate measures of fitness (r and lambda), and empirical studies, which mainly use lifetime reproductive success (LRS), or some of its correlates, as a fitness measure. We measured phenotypic selection on age-specific fertilities in three pre-modern human populations using individually estimated finite rate of increase, er (lambda). We found that lambda and lifetime reproductive success ranked individuals differently according to their fitness: for example, a female giving birth to four children at a young age may actually have a higher fitness than a female giving birth to six children at a greater age. Increase in fertility at the young age classes (15-19 years) was favoured by selection, but the intensity of selection on fertility was higher in the older age classes (20-30 years), where the variance in fertility was highest. Hence, variation in fertility in the older age classes (20-30) was actually responsible for most of the observed variation in fitness among the individuals. Additionally, more than 90% of variation in fitness (lambda) was attributable to individual differences in LRS, whereas only about 5% of all variation in fitness was due to differences in the reproductive schedule. The rate-sensitive fitness measure did not significantly challenge the importance of total fertility as a component of fitness in humans. However, the rate-sensitive measure clearly allowed more accurate estimation of individual fitness, which may be important for answering some more specific questions.     

Insecticide resistance enhances male reproductive success in a beetle

Abstract.— Malathion-specific resistance in the red flour beetle, Tribolium castaneum , is widespread and stable in natural populations even in the absence of pesticide exposure. To understand this stability, both resistant and susceptible males were placed in competition for susceptible female fertilization. Females were then isolated and their progeny was tested for malathion susceptibility. Male reproductive success was estimated for populations originating from different geographic areas and for isogenic strains. In most cases, resistant males had a greater reproductive success rate than susceptibles. The results suggest that male reproductive success is not traded against the selection for malathion resistance, even resistant individuals are at an advantage for this fitness trait. This absence of fitness cost may be the result of postselection of (1) modifier gene which ameliorate the fitness of resistant individuals or (2) nondeleterious resistance gene. Resistant phenotype superiority could be due to increased male mating success, improved ability of resistant males in sperm competition, female mate choice, and/or cryptic female choice of resistance gene(s). The effect of male phenotypic frequency on male reproductive success was also examined. We observed that male fertilization success is frequency dependent and inversely related to their frequency. However, this "rare male" advantage did not counteract the superiority of the resistant males.     

Determining the adaptive potential of maternal stress

Ecological and medical researchers are investing great effort to determine the role of Maternally‐Derived Stress (MDS) as an inducer of phenotypic plasticity in offspring. Many researchers have interpreted phenotypic responses as unavoidable negative outcomes (e.g., small birth weight, high anxiety); however, a biased underestimate of the adaptive potential of MDS‐induced effects is possible if they are not viewed within an ecologically relevant or a life‐history optimization framework. We review the ecological and environmental drivers of MDS, how MDS signals are transferred to offspring, and what responses MDS induces. Results from four free‐living vertebrate systems reveals that although MDS induces seemingly negative investment trade‐offs in offspring, these phenotypic adjustments can be adaptive if they better match the offspring to future environments; however, responses can prove maladaptive if they unreliably predict (i.e., are mismatched to) future environments. Furthermore, MDS‐induced adjustments that may prove maladaptive for individual offspring can still prove adaptive to mothers by reducing current reproductive investment, and benefitting lifetime reproductive success. We suggest that to properly determine the adaptive potential of MDS, researchers must take a broader integrated life‐history perspective, appreciate both the immediate and longer term environmental context, and examine lifetime offspring and maternal fitness.     

Differences in the temporal dynamics of phenotypic selection among fitness components in the wild

The balance of selection acting through different fitness components (e.g. fecundity, mating success, survival) determines the potential tempo and trajectory of adaptive evolution. Yet the extent to which the temporal dynamics of phenotypic selection may vary among fitness components is poorly understood. Here, we compiled a database of 3978 linear selection coefficients from temporally replicated studies of selection in wild populations to address this question. Across studies, we find that multi-year selection through mating success and fecundity is stronger than selection through survival, but varies less in direction. We also report that selection through mating success varies more in long-term average strength than selection through either survival or fecundity. The consistency in direction and stronger long-term average strength of selection through mating success and fecundity suggests that selection through these fitness components should cause more persistent directional evolution relative to selection through survival. Similar patterns were apparent for the subset of studies that evaluated the temporal dynamics of selection on traits simultaneously using several different fitness components, but few such studies exist. Taken together, these results reveal key differences in the temporal dynamics of selection acting through different fitness components, but they also reveal important limitations in our understanding of how selection drives adaptive evolution.