Suboptimal timing of reproduction in Lobelia inflata may be a conservative bet-hedging strategy

Age and size at reproduction are important components of fitness, and are variable both within and among angiosperm species. The fitness consequences of such life-history variation are most readily studied in organisms that reproduce only once in their lifetime. The timing of the onset of reproduction (bolting) in the monocarpic perennial, Lobelia inflata, occurs over a range of dates within a season, and may be postponed to a later year. Empirical relationships among life-history traits, derived from over 950 wild-growing and experimentally manipulated plants in the field, are used to model an optimal changing size threshold (norm of reaction) for bolting over the growing season. Comparisons are made between observed and expected norms of reaction governing bolting. An apparently suboptimal bolting schedule that precludes bolting beyond an early (conservative) date is observed, and is found to be qualitatively consistent with conservative bet hedging under unpredictable season lengths. On this basis we propose the schedule of bolting as a plausible example of a conservative bet-hedging strategy. The results underscore the critical need for long-term studies of fluctuating selection to distinguish suboptimality from bet hedging.     

Latitudinal variation in seed weight and flower number in Prunella vulgaris

Studies of seed-weight variation across altitudinal and latitudinal gradients have led to conflicting hypotheses regarding the selective value of this traint in relation to the length of the growing season. Growing-season length may also influence the evolution of seed number, and population differentiation in seed weight may be constrained by a negative genetic correlation between seed weight and seed number within populations. We examined variation in seed weight and an estimate of seed number (flower number) and the covariance of these traits among populations of Prunella vulgaris at five latitudes between northern Michigan and South Carolina. We measured seed weight and flower number in native habitats and in a common environment to determine the extent to which patterns observed in the field reflect genetic differentiation. We observed no genetically based variation in seed weight across the latitudinal gradient, although genetic variation among populations within a latitude was observed. In contrast to the lack of variation in seed weight, flower number increased clinally from northern Michigan to Tennessee in a common environment. Population mean flowering date in a common environment was successively later from north to south. Later-flowering individuals appear to achieve a larger size before flowering and consequently possess more resources for seed production. This difference may account for the greater flower production of late-flowering, southern populations. Independence of population mean seed weight and flower number across the latitudinal gradient suggests that population differentiation in seed weight has not been constrained by a trade-off between seed size and number within populations.     

Selection for increased allocation to offspring number under environmental unpredictability

According to life-history theory, the evolution of offspring size is constrained by the trade-off between allocation of resources to individual offspring and the number of offspring produced. Existing models explore the ecological consequences of offspring size, whereas number is invariably treated simply as an outcome of the trade-off with size. Here I ask whether there is a direct evolutionary advantage of increased allocation to offspring number under environmental unpredictability. Variable environments are expected to select for diversification in the timing of egg hatch and seed germination, yet the dependence of the expression of diversification strategies, and thus parental fitness, on offspring number has not previously been recognized. I begin by showing that well-established sampling theory predicts that a target bethedging diversification strategy is more reliably achieved as offspring number increases. I then use a simulation model to demonstrate that higher offspring number leads to greater geometric mean fitness under environmental uncertainty. Natural selection is thus expected to act directly to increase offspring number under assumptions of environmental unpredictability in season quality.     

Size and architectural traits as ontogenetic determinants of fitness in a phenotypically plastic annual weed (Amaranthus albus)

Abstract Plasticity of size and architectural traits, and their importance to reproductive fitness, were estimated in relation to nutrient availability in the annual Amaranthus albus . Seeds from seven field-collected genotypes were used to rear a first generation under uniform conditions. Seed families (inbred lines) from four first-generation plants per genotype were used to rear a second generation in a glasshouse for 10 weeks. Nine plants per family were regularly fertilized, while nine others were unfertilized. Size was estimated at 5, 8, and 10 weeks; architectural traits were recorded at 8 weeks (no. branches) and 10 weeks (no. branches and branch length). Fitness was assessed by the number of seeds per plant. Because traits were intercorrelated, size-scaled architectural traits were generated and allometric analyses performed. Genetic variation was analyzed for the second generation among inbred lines of the original genotypes, and among families within each genotype. For fertilized and unfertilized groups, early size (volume occupied at 5 weeks) and branch length per mass were significant determinants of fitness. The number of branches per size explained a smaller proportion of the variance in fitness. Genotype by treatment interaction was apparent for some traits, indicating genetic variation for plasticity, but plasticity of size did not change over ontogeny. Significant effects of genotype on size and architectural traits, and fitness, were detected mostly in the unfertilized group. Thus, selection is most likely to differentiate among genotypes in nutrient-poor environments. Lengthening of multiple branches increases seed output throughout the season, and genotypes with longer branches per unit mass have a selective advantage. Because early size is correlated with seed output, ontogenetic plasticity in response to improved soil resources allows opportunistic increases in fitness.     

The role of fungal pathogens in flower size and seed mass variation in three species of Hydrophyllum (Hydrophyllaceae)

Identifying ecological factors that affect seed number and seed size is key to understanding the persistence of large seed mass variation in some plant species. Pathogens may increase seed mass variation by increasing resource demand over the growing season such that late fruits experience higher resource competition than early fruits. We tested whether Fusarium sp. and Rhizoctonia sp., soil fungi that cause wilt, contributed to seasonal decline in flower size, seed number, or seed mass in Hydrophyllum appendiculatum and H. canadense. A third species not infected by these soil fungi, H. virginianum, was studied to determine how seasonal decline in floral traits and seed mass variation varies within this genus. Flower size declined seasonally for all species, but was greatest for H. appendiculatum, a monocarpic biennial with indeterminate inflorescences. Seed number decreased between first and last inflorescences in H. appendiculatum, but not in H. canadense or H. virginianum, perennials with determinate inflorescences. Seed mass varied most in H. appendiculatum and H. canadense (4-20-fold in 50% of individuals) and least in H. virginianum (4-8-fold in >30% of individuals). Fungal infection increased seed mass variation among diseased plants in H. canadense and H. appendiculatum. However, within plants fungal infection only increased seasonal decline in flower size, seed number, and seed mass in H. appendiculatum when flowers received supplemental pollination.     

Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards

The timing of birth is often correlated with offspring fitness in animals, but experimental studies that disentangle direct effects of parturition date and indirect effects mediated via variation in female traits are rare. In viviparous ectotherms, parturition date is largely driven by female thermal conditions, particularly maternal basking strategies. Our field and laboratory studies of a viviparous lizard (Niveoscincus ocellatus) show that earlier‐born offspring are more likely to survive through their first winter and are larger following that winter, than are later‐born conspecifics. Thus, the association between parturition date and offspring fitness is causal, rather than reflecting an underlying correlation between parturition date and maternal attributes. Survival selection on offspring confers a significant advantage for increased maternal basking in this species, mediated through fitness advantages of earlier parturition. We discuss the roles of environmentally imposed constraints and parent–offspring conflict in the evolution of maternal effects on parturition date.     

Reproductive compensation

The reproductive compensation hypothesis says that individuals constrained by ecological or social forces to reproduce with partners they do not prefer compensate for likely offspring viability deficits. The reproductive compensation hypothesis assumes that (i) pathogens and parasites evolve more rapidly than their hosts, (ii) mate preferences predict variation in health and viability of offspring, (iii) social and ecological factors keep some individuals from mating with their preferred partners (some are constrained to mate with partners they do not prefer), (iv) all individuals may be induced to compensate, so that (v) variation in compensation is due to environmental and developmental factors affecting between-individual abilities to express compensatory mechanisms. Selection favouring compensation may act through variation in prezygotic physiological mechanisms, zygotic mechanisms, or parental care to eggs or young that enhance offspring health, increasing the likelihood that some offspring survive to reproductive age, often at a survival cost to the parents. Compensation may be through increased number of eggs laid or offspring born, a compensatory effort working during a single reproductive bout that sometimes will match the number of offspring surviving to reproductive age produced by unconstrained parents during the same bout. The reproductive compensation hypothesis therefore predicts trade-offs in components of fitness for breeders, such that parents constrained to mating with a nonpreferred partner, but who compensate sometimes match their current productivity (number of offspring at reproductive age) to unconstrained parents (those breeding with their preferred partners), and, when all else is equal, die faster than unconstrained parents. The reproductive compensation hypothesis emphasizes that reproductive competition is not just between constrained and unconstrained individuals, but also among constrained individuals who do and do not compensate. The reproductive compensation hypothesis may thus explain previously unexplained between-population and within-population, between-individual variation in reproductive success, survival, physiology and behaviour.     

Sources and consequences of seed size variation in Lupinus perennis (Fabaceae): adaptive and non-adaptive hypotheses

Seed size variation within species and individuals is common. This variation may be adaptive in heterogeneous landscapes if the fitness consequences of seed size differ among environments or through time. Variation may also arise from constraints that limit control of seed size. I manipulated resource availability in both maternal and offspring environments to test conditions underlying these explanations for seed size variation in the herbaceous perennial Lupinus perennis. A fivefold variation in seed size arose primarily from differences among individuals and within-plant variability rather than from environmental conditions manipulated in the experiment. Environmental conditions had little effect on mean seed size; in contrast, within-plant variation in seed size increased with reduced resources. Fitness benefits from large seed size were similar across offspring environments, suggesting that environmental heterogeneity alone may not maintain seed size variation in this species. Surprisingly, seed size affected long-term fitness measures, including a plant's size and probability of flowering through its second year. These results are consistent with non-adaptive but not adaptive explanations for seed size variation. They also suggest that offspring size variation per se may contribute to variation in maternal fitness.     

Antagonistic pleiotropy can maintain fitness variation in annual plants

Antagonistic pleiotropy (AP) is a genetic trade‐off between different fitness components. In annual plants, a trade‐off between days to flower (DTF) and reproductive capacity often determines how many individuals survive to flower in a short growing season, and also influences the seed set of survivors. We develop a model of viability and fecundity selection informed by many experiments on the yellow monkeyflower, Mimulus guttatus, but applicable to many annual species. A viability/fecundity trade‐off maintains stable polymorphism under surprisingly general conditions. We also introduce both spatial heterogeneity and temporal stochasticity in environmental parameters. Neither is necessary for polymorphism, but spatial heterogeneity allows polymorphism while also generating the often observed non‐negative correlations in fitness components.     

Unexpected positive and negative effects of continuing inbreeding in one of the world's most inbred wild animals

Inbreeding depression, the reduced fitness of offspring of related individuals, is a central theme in evolutionary biology. Inbreeding effects are influenced by the genetic makeup of a population, which is driven by any history of genetic bottlenecks and genetic drift. The Chatham Island black robin represents a case of extreme inbreeding following two severe population bottlenecks. We tested whether inbreeding measured by a 20‐year pedigree predicted variation in fitness among individuals, despite the high mean level of inbreeding and low genetic diversity in this species. We found that paternal and maternal inbreeding reduced fledgling survival and individual inbreeding reduced juvenile survival, indicating that inbreeding depression affects even this highly inbred population. Close inbreeding also reduced survival for fledglings with less‐inbred mothers, but unexpectedly improved survival for fledglings with highly inbred mothers. This counterintuitive interaction could not be explained by various potentially confounding variables. We propose a genetic mechanism, whereby a highly inbred chick with a highly inbred parent inherits a “proven” genotype and thus experiences a fitness advantage, which could explain the interaction. The positive and negative effects we found emphasize that continuing inbreeding can have important effects on individual fitness, even in populations that are already highly inbred.     

Sex‐biased seed predation in gynodioecious Dianthus superbus var. longicalycinus (Capryophyllaceae) and differential influence of two seed predator species on the floral traits

Gynodioecy, the co‐occurrence of hermaphrodite and female individuals within a species, is maintained by differential reproductive success between sexes. Recently, researchers recognized that not only pollinators but also herbivores are important agents in the evolution and maintenance of gynodioecy, when herbivory is hermaphrodite biased. In this study, we investigated whether there is hermaphrodite‐biased herbivory in a gynodioecious plant, Dianthus superbus var. longicalycinus, and if so, what floral traits influenced hermaphrodite‐biased herbivory. We measured flower morphology (flower diameter, calyx tube length, corolla height and petal width) and phenology of flowers of female individuals, hermaphrodites and gynomonoecious individuals in a natural population. We also investigated seed predation and predator species. At the study site, Sibinia weevils (Curculionidae; Coleoptera) and Coleophora moths (Coleophoridae; Lepidoptera) were common pre‐dispersal seed predators in this species. The weevil appeared early in the flowering season, and weevil predation correlated with flower phenology. Because female individuals did not flower early in the season, weevil predation was less frequent in female individuals. Moth predation correlated with calyx length. The calyx length of flowers of female individuals was smaller than those of hermaphrodites, but a direct comparison of moth predation rates failed to find a significant difference among sex morphs. We found that the two seed predators had different effects on floral traits in D. superbus var. longicalycinus. We suggest that weevil predation contributes to the maintenance of gynodioecy because female individuals successfully escaped weevil predation by flowering late. It remains unclear why flower phenology is different among sex morphs.     

How should parents adjust the size of their young in response to local environmental cues?

Models of parental investment typically assume that populations are well mixed and homogeneous and have devoted little attention to the impact of spatial variation in the local environment. Here, in a patch‐structured model with limited dispersal, we assess to what extent resource‐rich and resource‐poor mothers should alter the size of their young in response to the local environment in their patch. We show that limited dispersal leads to a correlation between maternal and offspring environments, which favours plastic adjustment of offspring size in response to local survival risk. Strikingly, however, resource‐poor mothers are predicted to respond more strongly to local survival risk, whereas resource‐rich mothers are predicted to respond less strongly. This lack of sensitivity on the part of resource‐rich mothers is favoured because they accrue much of their fitness through dispersing young. By contrast, resource‐poor mothers accrue a larger fraction of their fitness through philopatric young and should therefore respond more strongly to local risk. Mothers with more resources gain a larger share of their fitness through dispersing young partly because their fitness in the local patch is constrained by the limited number of local breeding spots. In addition, when resource variation occurs at the patch level, the philopatric offspring of resource‐rich mothers face stronger competition from the offspring of other local mothers, who also enjoy abundant resources. The effect of limited local breeding opportunities becomes less pronounced as patch size increases, but the impact of patch‐level variation in resources holds up even with many breeders per patch.     

Trait biogeography of marine copepods – an analysis across scales

Functional traits, rather than taxonomic identity, determine the fitness of individuals in their environment: traits of marine organisms are therefore expected to vary across the global ocean as a function of the environment. Here, we quantify such spatial and seasonal variations based on extensive empirical data and present the first global biogeography of key traits (body size, feeding mode, relative offspring size and myelination) for pelagic copepods, the major group of marine zooplankton. We identify strong patterns with latitude, season and between ocean basins that are partially (c. 50%) explained by key environmental drivers. Body size, for example decreases with temperature, confirming the temperature‐size rule, but surprisingly also with productivity, possibly driven by food‐chain length and size‐selective predation. Patterns unrelated to environmental predictors may originate from phylogenetic clustering. Our maps can be used as a test‐bed for trait‐based mechanistic models and to inspire next‐generation biogeochemical models.     

Pollen colour morphs take different paths to fitness

Colour phenotypes are often involved in communication and are thus under selection by species interactions. However, selection may also act on colour through correlated traits or alternative functions of biochemical pigments. Such forms of selection are instrumental in maintaining petal colour diversity in plants. Pollen colour also varies markedly, but the maintenance of this variation is little understood. In Campanula americana, pollen ranges from white to dark purple, with darker morphs garnering more pollinator visits and exhibiting elevated pollen performance under heat stress. Here, we generate an F2 population segregating for pollen colour and measure correlations with floral traits, pollen attributes and plant‐level traits related to fitness. We determine the pigment biochemistry of colour variants and evaluate maternal and paternal fitness of light and dark morphs by crossing within and between morphs. Pollen colour was largely uncorrelated with floral traits (petal colour, size, nectar traits) suggesting it can evolve independently. Darker pollen grains were larger and had higher anthocyanin content (cyanidin and peonidin) which may explain why they outperform light pollen under heat stress. Overall, pollen‐related fitness metrics were greater for dark pollen, and dark pollen sires generated seeds with higher germination potential. Conversely, light pollen plants produce 61% more flowers than dark, and 18% more seeds per fruit, suggesting a seed production advantage. Results indicate that light and dark morphs may achieve fitness through different means—dark morphs appear to have a pollen advantage whereas light morphs have an ovule advantage—helping to explain the maintenance of pollen colour variation.     

Male and female effects on fertilization success and offspring viability in the Peron's tree frog,Litoria peronii

Abstract There is increasing theoretical and empirical evidence that genetic compatibility among partners is an important determinant of fertilization success and offspring viability. In amphibians, females often actively choose partners from among a variety of males and polyandry is common. Genetic compatibility among partners may therefore be an important determinant of fertilization success and offspring viability in some amphibians. Amphibians also show some of the highest levels of genetic differentiation among neighbouring populations known in vertebrates, and as such, populations may have evolved different co‐adapted gene complexes. This means that offspring from among‐population crosses may have reduced fitness. It is therefore essential to understand to what extent crossings between and within populations may interfere with successful fertilization and offspring viability. Here, we test whether crossing individuals within and between two different populations of the Australian Peron's tree frog (Litoria peronii) using artificial fertilizations affect fertilization success and offspring viability. Fertilization success per se is strongly influenced by male identity, which is likely to depend at least to some extent on the experimental procedure (e.g. resulting in variation in sperm number per ejaculate), whereas there was no fertilization effect of female identity. More importantly, male and female identity, independently of each other, explained significant variation in offspring viability, whereas no such effect could be linked to population of origin. Thus, our experiments suggest that crossing populations may not always be the most significant factor affecting fertilization success or offspring viability, but may be more influenced by the genetic quality or the genetic compatibility of partners.     

Hierarchical pre-dispersal fitness assessment in a Mediterranean shrub plant

Under the concept of modularity, it is possible to recognise how seed production, as well as any other process affecting it, are hierarchically structured within fruits, within individual plants and within populations. In this work, we analysed the effects of pre-dispersal seed predation by insects upon a set of hierarchical levels in a population of the Mediterranean shrub plant Cistus ladanifer (“rock rose”) throughout a complete fruit-producing season (which takes place during the summer months). Almost all individual plants were predated, which implies that the effects of predation at the population level (regardless of the extent of predation within each individual) were virtually uniform. Within the individuals, however, the predation rate was close to a proportion of 0.5 (half of the fruits of each individual were predated), which indicates that this hierarchical level is likely to be subjected to a differential action of selection. Predation rates within the fruits showed an intermediate value (lower than that observed at the population level but higher than that at the individual level). According to these results, the pressure of phenotypic selection may therefore give rise to greater variation among fruits of the same individual than among seeds of the same fruit. In terms of the temporal patterns observed there was a large variation in the increments of predation along the fruiting season, which implies a high degree of heterogeneity in the temporal distribution of the effects of predation pressure on fitness. Besides its use in the specific example of the plant species studied in this work, the methodological procedure presented in this paper (integration of the temporal changes of different hierarchical levels) might be foreseen, in fact, as a useful tool for analysing the hierarchical structuring of fitness in modular organisms in general. This procedure allows to discriminate and integrate selection pressures and their effects across different phenotypic levels, from the infra-individual ones up to the population level.     

The role of the tolerance–fecundity trade‐off in maintaining intraspecific seed trait variation in a widespread dimorphic herb

Coexistence of species with different seed sizes is a long‐standing issue in community ecology, and a trade‐off between fecundity and stress tolerance has been proposed to explain co‐occurrence in heterogeneous environments. Here we tested an intraspecific extension of this model: whether such trade‐off also explains seed trait variation among populations of widespread plants under stress gradients. We collected seeds from 14 populations of Plantago coronopus along the Atlantic coast in North Africa and Europe. This herb presents seed dimorphism, producing large basal seeds with a mucilaginous coat that facilitates water absorption (more stress tolerant), and small apical seeds without coats (less stress tolerant). We analysed variation among populations in number, size and mucilage production of basal and apical seeds, and searched for relationships between local environment and plant size. Populations under higher stress (higher temperature, lower precipitation, lower soil organic matter) had fewer seeds per fruit, higher predominance of basal relative to apical seeds, and larger basal seeds with thicker mucilaginous coats. These results strongly suggest a trade‐off between tolerance and fecundity at the fruit level underpins variation in seed traits among P. coronopus populations. However, seed production per plant showed the opposite pattern to seed production per fruit, and seemed related to plant size and other life‐cycle components, as an additional strategy to cope with environmental variation across the range. The tolerance–fecundity model may constitute, under stress gradients, a broader ecological framework to explain trait variation than the classical seed size–number compromise, although several fecundity levels and traits should be considered to understand the diverse strategies of widespread plants to maximise fitness in each set of local conditions.     

Impact of Culm Harvest on Seed Production in a Monocarpic Bamboo

Successful regeneration of bamboos from seed is a key issue in the ecology of many tropical regions and the livelihoods of their inhabitants. The gregarious monocarpy of many bamboos may be driven by a need to satiate seed predators by seeding in abundance at infrequent intervals. In long‐lived clonal monocarps, seed production is expected to be positively related to the success of the clone in generating more and larger ramets during its lifetime. Ramification may be constrained by harvesting of culms, but it is unclear whether the reduction in productivity is proportional to the loss of reproductive biomass. We counted the seed produced by 661 culms (ramet stems) sampled from 90 clumps of the gregariously monocarpic bamboo Schizostachyum dullooa that is intensively harvested by villagers in northeastern India. The smallest clumps had fewer culms and few or no culms more than one year old. Seed production was indeed positively related to culm size and the number of culms in a clump. First‐year culms were markedly more productive than older culms after controlling for culm diameter and clump size. There was a negative effect of clump size on productivity per culm which may occur because clumps that had been harvested heavily were able to exploit resources retained in rhizomes from harvested culms. Nevertheless, small clumps produced much less seed than larger clumps, generating a risk of unknown magnitude that heavily harvested stands of monocarpic bamboos may be unable to satiate seed predators during their single opportunity for reproduction.     

The effects of fire on scarlet gilia: an alternative selection pressure to herbivory?

Summary The primary goals of this paper were to experimentally assess the relative importance of fire, a potentially important selective agent involved in shaping scarlet gilia's compensatory response and, in general, determine scarlet gilia's response to fire. Burn treatment results demonstrated that fire was not an important selective agent involved in shaping scarlet gilia's compensatory response. The most common response to fire was the production of one or more new clonally derived rosettes. This was an unexpected result; this typically monocarpic herb rarely produces clonal offspring. Although rosette production lessened the detrimental effects of fire by giving plants that cloned a second chance to flower, these newly formed rosettes delayed flowering for at least one year and had significantly higher overwinter mortality rates than rosettes from unburned control plots. In addition, significantly fewer individuals from the burn treatments flowered and there was significantly higher immediate mortality. There was, however, no detrimental effect on the reproductive success (seed production) of individuals that flowered following the burn. Overall, cumulative estimates of plant performance suggest that at the population level fire results in a 4.5-fold decrease in relative plant fitness. However, fire-induced seed germination could negate the detrimental effects of fire on the population dynamics of scarlet gilia. In the year of the burn there was a 116-fold increase in the number of germinating seeds and by the second year this translated into an approximate 6-fold difference in the number of surviving rosettes. Two alternative candidates, frost damage and ungulate trampling, can cause the removal of apical dominance and a response similar to that generated by ungulate and insect herbivores. However, they are probably minor factors favoring selection toward growth compensation; experimental and observational results deomonstrate that apical dominance was removed in only 3% of plants exposed to freezing temperatures and ungulate trampling caused breakage and release of apical dominance in only 0.2% of plants.