Variable timing of reproduction in unpredictable environments: adaption of flood plain plants

We study the evolutionarily stable reproductive timing of annual plants that face unpredictable environmental disturbances. Plants living in a riverbed often experience a disturbance before they reproduce, suffering major fitness loss. Plants reproducing prior to the flood season are free from the risk of lost reproduction, but a small flowering plant can produce only a few numbers of seeds. If the date of disturbance is unpredictable, a mixed strategy of reproductive timing may evolve in which individuals of the same genotype have different reproductive dates. We calculate the evolutionarily stable phenotype distribution analytically. Depending on parameters, the ESS distribution is either (1) a timid strategy-the plant reproduces when small, prior to the major disturbance season; (2) a bold strategy-the plant reproduces only when it is fully grown; (3) a mixture of early and late reproduction; or (4) dates of reproduction spread over a wide interval. We also examine the effects of developmental and environmental noises that make realized flowering dates deviate from that programmed by the genotype, which follows the ESS distribution. In the presence of noise, the ESS distribution of programmed timing of reproduction is discrete.     

Nonvulnerability of ecosystems in unpredictable environments

One way to bracket the effects of a real environment on an ecosystem during a finite time interval is to use the concept of vulnerability. If a deterministic model ecosystem has a good Lyapunov function, it may be possible to derive simple and useful tests for the system to be nonvulnerable. For a subset of Lotka-Volterra models, the system is nonvulnerable if the smallest eigenvalue of a certain matrix is not only positive, but is greater than a positive number, which depends on a priori estimates for the bounds on the unpredictable forcing functions. The bounded but unknown functions which act on the Lotka-Volterra equations also can be interpreted as errors in the system's equations which can be tolerated without a qualitative change in the behaviour of its solutions.     

Population differentiation of temperate amphibians in unpredictable environments

Amphibians are a globally distributed and diverse lineage, but much of our current understanding of their population genetic structure comes from studies in mesic temperate habitats. We characterize the population genetic structure of two sympatric explosive breeding amphibians in the southwestern deserts of the United States: the Great Plains toad ( Anaxyrus cognatus ) and Couch's spadefoot toad ( Scaphiopus couchii ). For both species, we find limited genetic differentiation even between populations in adjacent valleys separated by dispersal barriers such as mountainous habitats. To understand how population genetic patterns in these two arid-adapted species compare to taxa in more mesic environments, we computed a standardized measure of population differentiation for A. cognatus , S. couchii , and for pond-breeding amphibians that inhabit mesic temperate environments. Our results indicate that the arid-adapted species have lower population genetic structure at fine and moderate scales than most other amphibian species we surveyed. We hypothesize that stochasticity in the availability of appropriate breeding sites as well as landscape homogeneity may result in increased population connectivity in desert-adapted frogs. Future work examining fine-scale population structure in amphibians from a diversity of habitats will test the generality of our findings. Intraspecific comparisons among localities with varied seasonality and habitats will be particularly useful for investigating the interaction between species-typical population dynamics and environmental characteristics as determinants of population connectivity in pond-breeding amphibians.     

Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction

Adaptation in dynamic environments depends on the grain, magnitude and predictability of ecological fluctuations experienced within and across generations. Phenotypic plasticity is a well-studied mechanism in this regard, yet the potentially complex effects of stochastic environmental variation on optimal mean trait values are often overlooked. Using an optimality model inspired by timing of reproduction in great tits, we show that temporal variation affects not only optimal reaction norm slope, but also elevation. With increased environmental variation and an asymmetric relationship between fitness and breeding date, optimal timing shifts away from the side of the fitness curve with the steepest decline. In a relatively constant environment, the timing of the birds is matched with the seasonal food peak, but they become adaptively mismatched in environments with temporal variation in temperature whenever the fitness curve is asymmetric. Various processes affecting the survival of offspring and parents influence this asymmetry, which collectively determine the 'safest' strategy, i.e. whether females should breed before, on, or after the food peak in a variable environment. As climate change might affect the (co)variance of environmental variables as well as their averages, risk aversion may influence how species should shift their seasonal timing in a warming world.     

Circannual clocks in avian reproduction and migration

Many behavioural and physiological functions of organisms are adjusted to the periodic changes in their environment, particularly to those related to the natural day and year. This adjustment is often achieved through the action of endogenous daily (circadian) and annual (circannual) clocks. Studies of the control of avian moult, migration and reproduction have played a major role in understanding how biological clocks function and interact with rhythms in the environment. Investigations on tropical birds such as the East African subspecies of the Stonechat ( Saxicola torquata axillaris ). and long-distance migrants like the Garden Warbler ( Sylvia borin ). have provided the longest records of circannual rhythms, some of them running for more than 12 years, with periods ranging from about 9 to 13 months. Avian circannual rhythms are organized in a characteristic way for a particular species or population, and cross-breeding experiments have shown that some of the differences found among them are genetically determined. In African Stonechats circannual rhythms guarantee that seasonal events occur at the appropriate times of the year and in the characteristic sequence. They also control a "reproductive window" that provides the temporal framework for breeding. The width of this window is rather inflexible but the performance of a bird within this framework (e.g. whether it breeds once or twice per season) is subject to modification by environmental conditions. In migratory birds circannual programs are involved in determining the time course, distance and direction of migration. Circannual rhythms are synchronized with and modified by environmental factors in a complex way, but the endogenous mechanisms usually respond to environmental cues such that an optimal adjustment to season and latitude is guaranteed.     

Circannual clocks in avian reproduction and migration

Many behavioural and physiological functions of organisms are adjusted to the periodic changes in their environment, particularly to those related to the natural day and year. This adjustment is often achieved through the action of endogenous daily (circadian) and annual (circannual) clocks. Studies of the control of avian moult, migration and reproduction have played a major role in understanding how biological clocks function and interact with rhythms in the environment. Investigations on tropical birds such as the East African subspecies of the Stonechat ( Saxicola torquata axillaris ) and long-distance migrants like the Garden Warbler ( Sylvia boriri ) have provided the longest records of circannual rhythms, some of them running for more than 12 years, with periods ranging from about 9 to 13 months. Avian circannual rhythms are organized in a characteristic way for a particular species or population, and cross-breeding experiments have shown that some of the differences found among them are genetically determined. In African Stonechats circannual rhythms guarantee that seasonal events occur at the appropriate times of the year and in the characteristic sequence. They also control a "reproductive window" that provides the temporal framework for breeding. The width of this window is rather inflexible but the performance of a bird within this framework (e.g. whether it breeds once or twice per season) is subject to modification by environmental conditions. In migratory birds circannual programs are involved in determining the time course, distance and direction of migration. Circannual rhythms are synchronized with and modified by environmental factors in a complex way, but the endogenous mechanisms usually respond to environmental cues such that an optimal adjustment to season and latitude is guaranteed.     

Solar activity affects avian timing of reproduction

Avian timing of reproduction is strongly affected by ambient temperature. Here we show that there is an additional effect of sunspots on laying date, from five long-term population studies of great and blue tits (Parus major and Cyanistes caeruleus), demonstrating for the first time that solar activity not only has an effect on population numbers but that it also affects the timing of animal behaviour. This effect is statistically independent of ambient temperature. In years with few sunspots, birds initiate laying late while they are often early in years with many sunspots. The sunspot effect may be owing to a crucial difference between the method of temperature measurements by meteorological stations (in the shade) and the temperatures experienced by the birds. A better understanding of the impact of all the thermal components of weather on the phenology of ecosystems is essential when predicting their responses to climate change.     

Creosote growth rate and reproduction increase in postfire environments

Human activities are changing patterns of ecological disturbance globally. In North American deserts, wildfire is increasing in size and frequency due to fuel characteristics of invasive annual grasses. Fire reduces the abundance and cover of native vegetation in desert ecosystems. In this study, we sought to characterize stem growth and reproductive output of a dominant native shrub in the Mojave Desert, creosote bush (Larrea tridentata (DC.) Coville) following wildfires that occurred in 2005. We sampled 55 shrubs along burned and unburned transects 12 years after the fires (2017) and quantified age, stem diameter, stem number, radial and vertical growth rates, and fruit production for each shrub. The shrubs on the burn transects were most likely postfire resprouts based on stem age while stems from unburn transects dated from before the fire. Stem and vertical growth rates for shrubs on burned transects were 2.6 and 1.7 times higher than that observed for shrubs on unburned transects. Fruit production of shrubs along burned transects was 4.7‐fold more than shrubs along paired unburned transects. Growth rates and fruit production of shrubs in burned areas did not differ with increasing distance from the burn perimeter. Positive growth and reproduction responses of creosote following wildfires could be critical for soil stabilization and re‐establishment of native plant communities in this desert system. Additional research is needed to assess if repeat fires that are characteristic of invasive grass‐fire cycles may limit these benefits.     

The basic reproduction number $$R_0$$ in time-heterogeneous environments

Journal of Mathematical Biology - In the previous paper (Inaba in J Math Biol 65:309–348, 2012), we proposed a new (most biologically natural) definition of the basic reproduction number...     

Risky business: sexual and asexual reproduction in variable environments

Patterns of reproductive uncertainty can have an important influence on population dynamics. There is a crucial distinction between what we describe here as aggregate uncertainty (in which reproductive output in each generation is correlated among the individuals in a population) and idiosyncratic risk (in which reproductive output is independent across individuals). All else being equal, populations experiencing idiosyncratic risk enjoy a higher asymptotic growth rate than do those experiencing aggregate uncertainty. Therefore individuals in populations of the former type will have a competitive advantage over individuals in populations of the latter type. Applying this distinction to models of randomly fluctuating environments, we point out that genetic variation among offspring can serve to reduce aggregate uncertainty, transforming it into a more idiosyncratic form of risk. We show that this transformation underlies the dynamics observed in several previous models of the role of outcrossing in the evolution of sex.     

Timing of current reproduction directly affects future reproductive output in European coots

Life-history theory suggests that the variation in the seasonal timing of reproduction within populations may be explained on the basis of individual optimization. Optimal breeding times would vary between individuals as a result of trade-offs between fitness components. The existence of such trade-offs has seldom been tested empirically. We experimentally investigated the consequences of altered timing of current reproduction for future reproductive output in the European coot (Fulica atra). First clutches of different laying date were cross-fostered between nests, and parents thereby experienced a delay or an advance in the hatching date. The probability and success of a second brood, adult survival until and reproduction in the next season were then compared to the natural variation among control pairs. Among control pairs the probability of a second brood declined with the progress of season. Delayed pairs were less likely and advanced pairs were more likely to produce a second brood. These changes were quantitatively as predicted from the natural seasonal decline. The number of eggs in the second clutch was positively related to egg number in the first clutch and negatively related to laying date. Compared to the natural variation, delayed females had more and advanced females had fewer eggs in their second clutch. The size of the second brood declined with season, but there was no significant effect of delay or advance. Local adult survival was higher following a delay and reduced following an advance. The effect of the experiment on adult survival was independent of sex. Laying date and clutch size of females breeding in the next year were not affected by treatment. The study demonstrates the existence of a trade-off between increased probability of a second brood and decreased parental survival for early breeding. Timing-dependent effects of current reproduction on future reproductive output may thus play an important role in the evolution of the seasonal timing of reproduction.     

The perfume of reproduction in birds: Chemosignaling in avian social life

This article is part of a Special Issue “Chemosignals and Reproduction”.Chemical cues were probably the first cues ever used to communicate and are still ubiquitous among living organisms. Birds have long been considered an exception: it was believed that birds were anosmic and relied on their acute visual and acoustic capabilities. Birds are however excellent smellers and use odors in various contexts including food searching, orientation, and also breeding. Successful reproduction in most vertebrates involves the exchange of complex social signals between partners. The first evidence for a role of olfaction in reproductive contexts in birds only dates back to the seventies, when ducks were shown to require a functional sense of smell to express normal sexual behaviors. Nowadays, even if the interest for olfaction in birds has largely increased, the role that bodily odors play in reproduction still remains largely understudied. The few available studies suggest that olfaction is involved in many reproductive stages. Odors have been shown to influence the choice and synchronization of partners, the choice of nest-building material or the care for the eggs and offspring. How this chemical information is translated at the physiological level mostly remains to be described, although available evidence suggests that, as in mammals, key reproductive brain areas like the medial preoptic nucleus are activated by relevant olfactory signals. Olfaction in birds receives increasing attention and novel findings are continuously published, but many exciting discoveries are still ahead of us, and could make birds one of the animal classes with the largest panel of developed senses ever described.     

Evolution of delayed reproduction in uncertain environments: a life-history perspective

Environmental uncertainty alone can select for delayed reproduction; however, its relative role in the evolution of delayed reproduction across life histories is not known. Along a life-history spectrum from low-survival/high-fertility species to high-survival/low-fertility species, we show that the latter are more likely to evolve delayed reproduction if fertility varies over time. By contrast, if survival varies over time, low-survival life histories are more likely to evolve delays. If there is variation in both survival and fertility, and if this variation is positively associated, the evolutionarily stable reproductive delay is decreased (relative to independent variation in survival and fertility). Conversely, if variation in survival and fertility is negatively associated, the evolutionarily stable reproductive delay is increased. We further show that environmental uncertainty can drive the evolution of delayed reproduction in an iteroparous organism but only in the special case where juvenile survival is greater than adult survival. For common iteroparous life histories (adult survival > juvenile survival), environmental uncertainty does not select for delayed reproduction. Thus, any benefits that delayed reproduction might have on reproduction or survival could be especially important in explaining the common observation of delayed reproduction in many vertebrates and perennial plants.     

Temperature has a causal effect on avian timing of reproduction

Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. We tested the direct effect of temperature on laying dates in great tits (Parus major) using climatized aviaries in a 6-year experiment. We mimicked the temperature patterns from two specific years in which our wild population laid either early (‘warm’ treatment) or late (‘cold’ treatment). Laying dates were affected by temperature directly. As the relevant temperature period started three weeks prior to the mean laying date, with a range of just 4°C between the warm and the cold treatments, and as the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. We furthermore show a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. Our results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.     

Phenotypic selection and regulation of reproduction in different environments in wild barley

Plasticity of the phenotypic architecture of wild barley, Hordeum spontaneum, was studied in response to water and nutrient stress. Direct and indirect selection on several vegetative and reproductive traits was estimated and path analysis used to reveal how regulating pathways via maternal investment differed between environments. Vegetative traits displayed differential regulating effect on fitness across experimental environments: (1) increase in size was selected for under optimal conditions and under water stress, but not under nutrient stress; (2) allocation to root biomass was selected for under optimal conditions, but it had no effect under nutrient stress and was strongly selected against when water was limiting; (3) delayed onset of reproduction was selected under nutrient limitation whereas earlier onset was selected under water stress. The regulating effect of reproductive traits on final reproductive output also differed across treatments, operating either at the 'early' stage of plant development through varying the number of initiated spikelets per spike (no stress and water stress treatment) or at the 'late' developmental stage adjusting the fertile spikelet weight (no stress and nutrient stress treatment). Reproductive output was regulated via seed abortion under no stress and water stress treatments. Although the underlying mechanism of the regulation through abortion has yet to be discovered, the specific mechanism of abortion under water stress appears to be different from that under optimal conditions. Our results demonstrate that not only is the character architecture in wild barley plastic and sensitive to changing availability of water and nutrients, but the regulating mechanism of maternal investment is also environmentally sensitive.