Isabel M. Smallegange

Towards a general, population-level understanding of eco-evolutionary change

Most population-level studies of eco-evolutionary dynamics assume that evolutionary change occurs in response to ecological change and vice versa. However, a growing number of papers report simultaneous ecological and evolutionary change, suggesting that the eco-evolutionary consequences of environmental change for populations can only be fully understood through the simultaneous analysis of statistics used to describe both ecological and evolutionary dynamics. Here we argue that integral projection models (IPM), and matrix approximations of them, provide a powerful approach to integrate population ecology, life history theory, and evolution. We discuss key questions in population biology that can be examined using these models, the answers to which are essential for a general, population-level understanding of eco-evolutionary change.

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.

Tits on the move: exploring the impact of environmental change on blue tit and great tit migration distance

1. In response to warmer spring conditions in Central Europe many migratory bird species have shifted their timing of breeding. Environmental change has also led to warmer winters, shortening the distance between the breeding grounds of migratory birds and their overwintering areas. 2. Here, we show that in response to warmer winters, blue tits (Cyanistes caeruleus), but not great tits (Parus major), breeding in Germany decreased their migration distance between 1964 and 1996. Understanding this difference provides insight into possible constraints and selection pressures involved in how species respond to environmental change. Here, we focus on their breeding ecology. 3. In a nest box population in southern Germany, both species laid their first clutch earlier with increasing spring temperature, but over the study period (1974-1999) blue tits showed a significant and stronger advancement in laying date than great tits. For both species, selection for earlier breeding did not vary with environmental change, indicating that early laying pairs did not do better than later laying pairs as spring temperature increased. 4. Blue tits in the nest box population were single-brooded and existing hypotheses state that single-brooded species likely advance their laying date to match timing of reproduction with the advancing food peak in spring. We hypothesize that this might be one reason why blue tits adjusted their migration strategy as closer proximity to the breeding grounds in winter allows better prediction of the onset of spring. Ten per cent of great tits successfully produced second broods and their first clutch laying date is a compromise between first and second clutch laying date, which might be why great tits had not advanced their laying date nor altered their migration strategy.

Food supply and demand, a simulation model of the functional response of grazing ruminants

A dynamic model of the functional response is a first prerequisite to be able to bridge the gap between local feeding ecology and grazing rules that pertain to larger scales. A mechanistic model is presented that simulates the functional response, growth and grazing time of ruminants. It is based on results of studies on voluntary food intake and animal production of ruminants. Physiological requirements and food quality are key factors that determine the intake. The model is also based on the results of studies on the functional response of grazers. Quantitative aspects of vegetations i.e. bulk density and height, and the animals’ mouth dimensions are the main factors that determine how much a grazer can swallow. The structure of the model applies to ruminants under tropical conditions. The model parameters are set and validated for the African buffalo, Syncerus caffer. Three variants of the model are elaborated: a non-reproducing female, a reproducing female and a male ruminant. The similarity between the results of the simulation runs and field data are considered to be satisfactory. The results suggest that the quality of the vegetation i.e. the crude protein content, together with the animals energy requirements, govern the daily intake of food. However, the quantitative characteristics of the vegetation, especially height, can be critical. The model aims to be a tool in the interpretation of empirical field data and in the development of grazing theory. Transparency, concision and a robust empirical basis were therefore striven after in the construction of the model.

The stochastic demography of two coexisting male morphs

Abstract. If genetically distinct morphs coexist under a range of natural conditions, they should have equal long-run fitnesses across a wide range of different stochastic environments. In other words, the sequence and frequency of good and bad environments should not substantially impact long-run growth rates. When different morphs have contrasting life histories that vary with environmental conditions, however, it seems improbable that growth rates can be equivalent across a range of stochastic environments without invoking a strong stabilizing mechanism to explain their persistence. As yet, there has been no research characterizing the long-run stochastic growth rate (lambdaS) of different morphs across a wide range of stochastic environments. Assuming density independence, we show that the two genetic male morphs in the bulb mite (Rhizoglyphus robini-fighters, which are able to kill other mites, and benign scramblers-have similar lambdas in different Markovian environments (different simulated random sequences of good and bad habitats). Elasticity analyses revealed that Xs was most sensitive to perturbation of adult survival rate. A slight (biologically and statistically realistic) increase in scrambler adult survival equalized scrambler and fighter X,. The fitness equivalence of the two morphs suggests that stabilizing mechanisms, such as density or frequency dependence, required to maintain their coexistence, are weak. We advocate that stochastic demography can offer a powerful approach to identify and understand the circumstances under which genetic polymorphisms can be maintained in stochastic environments.

Effects of paternal phenotype and environmental variability on age and size at maturity in a male dimorphic mite

Investigating how the environment affects age and size at maturity of individuals is crucial to understanding how changes in the environment affect population dynamics through the biology of a species. Paternal phenotype, maternal, and offspring environment may crucially influence these traits, but to my knowledge, their combined effects have not yet been tested. Here, I found that in bulb mites (Rhizoglyphus robini), maternal nutrition, offspring nutrition, and paternal phenotype (males are fighters, able to kill other mites, or benign scramblers) interactively affected offspring age and size at maturity. The largest effect occurred when both maternal and offspring nutrition was poor: in that case offspring from fighter sires required a significantly longer development time than offspring from scrambler sires. Investigating parental effects on the relationship between age and size at maturity revealed no paternal effects, and only for females was its shape influenced by maternal nutrition. Overall, this reaction norm was nonlinear. These non-genetic intergenerational effects may play a complex, yet unexplored role in influencing population fluctuations—possibly explaining why results from field studies often do not match theoretical predictions on maternal effects on population dynamics.

Mechanistic description of population dynamics using dynamic energy budget theory incorporated into integral projection models

Integral projection models (IPMs) provide a powerful approach to investigate ecological and rapid evolutionary change in quantitative life history characteristics and population dynamics. IPMs are constructed from functions that describe the demographic rates – survival, growth and reproduction – in relation to the characteristics of individuals and their environment. Currently, however, demographic rates are estimated using phenomenological regression models that lack a mechanistic representation of the biological processes that give rise to observed demographic variation. This lack of mechanistic underpinning limits the ability of the model to predict future dynamics under novel environmental conditions because the model ingredients pertain to current environmental conditions only. Here we use Dynamic Energy Budget (DEB) theory to construct DEB-IPMs based on a mechanistic representation of individual life history trajectories. We derive the demographic functions describing growth and reproduction from a simple DEB growth model. The functions describing mortality and the association between parent and offspring characteristics do not follow DEB theory, and hence are estimated from individual-level observations. We apply the DEB-IPM to two contrasting systems: the small, fast-reproducing bulb mite (Rhizoglyphus robini) and the large, slow-reproducing reef manta ray (Manta alfredi). In both cases, predictions of population growth rate, lifetime reproductive success and generation time agree with empirical observations. In case of the bulb mite, predictions and observations even agree across different feeding conditions. If the DEB energetics model is accepted as describing growth and reproduction, DEB-IPMs can be parameterised using easy-to-collect life cycle information (growth rate, length at birth, maturation and old age) making them suitable for data-deficient species. Because species differ only in these DEB parameters, comparative studies of character and population dynamics between species are straightforward, particularly since DEB-IPMs can be extended to include population feedback on resources, of which we give an example. Most crucially, because DEB theory specifies growth and reproduction rates as explicitly dependent on environmental conditions such as food availability or temperature, DEB-IPMs provide a mechanistic platform to investigate the biological processes that determine joint change in phenotypic characters, life history traits, population size and community structure. This article is protected by copyright. All rights reserved.

Eco-Evolutionary Interactions as a Consequence of Selection on a Secondary Sexual Trait

Ecological and evolutionary population changes are often interlinked, complicating the understanding of how each is affected by environmental change. Using a male dimorphic mite as a model system, we studied concurrent changes in the expression of a conditional strategy and in the population in response to harvesting over 15 generations. We found evolutionary divergence in the expression of alternative male reproductive morphs—fighters and defenceless scramblers (sneakers)—caused by the selective harvesting of each male morph. Regardless of which morph was targeted, the direction of evolution of male morph expression in response to harvesting was always towards scramblers, which, in case of the harvesting of scramblers, we attributed to strong ecological feedback (reduced cannibalism opportunities for fighters) within the closed populations. Current evolutionary theory, however, predicts that the frequency of a morph always decreases when selected against: to understand phenotypic trait evolution fully, evolutionary theory would benefit from including ecological interactions, especially if traits have ecological consequences that in turn feedback to their evolutionary trajectory.

Life-history differences favor evolution of male dimorphism in competitive games.

Many species exhibit two discrete male morphs: fighters and sneakers. Fighters are large and possess weapons but may mature slowly. Sneakers are small and have no weapons but can sneak matings and may mature quickly to start mating earlier in life than fighters. However, how differences in competitive ability and life history interact to determine male morph coexistence has not yet been investigated within a single framework. Here we integrate demography and game theory into a two-sex population model to study the evolution of strategies that result in the coexistence of fighters and sneakers. We incorporate differences in maturation time between the morphs and use a mating-probability matrix analogous to the classic hawk-dove game. Using adaptive dynamics, we show that male dimorphism evolves more easily in our model than in classic game theory approaches. Our results also revealed an interaction between life-history differences and sneaker competitiveness, which shows that demography and competitive games should be treated as interlinked mechanisms to understand the evolution of male dimorphism. Applying our approach to empirical data on bulb mites (Rhizoglyphus robini), coho salmon (Oncorhynchus kisutch), and bullhorned dung beetles (Onthophagus taurus) indicates that observed occurrences of male dimorphism are in general agreement with model predictions.

Correlative changes in life-history variables in response to environmental change in a model organism.

Global change alters the environment, including increases in the frequency of (un)favorable events and shifts in environmental noise color. However, how these changes impact the dynamics of populations, and whether these can be predicted accurately has been largely unexamined. Here we combine recently developed population modeling approaches and theory in stochastic demography to explore how life history, morphology, and average fitness respond to changes in the frequency of favorable environmental conditions and in the color of environmental noise in a model organism (an acarid mite). We predict that different life-history variables respond correlatively to changes in the environment, and we identify different life-history variables, including lifetime reproductive success, as indicators of average fitness and life-history speed across stochastic environments. Depending on the shape of adult survival rate, generation time can be used as an indicator of the response of populations to stochastic change, as in the deterministic case. This work is a useful step toward understanding population dynamics in stochastic environments, including how stochastic change may shape the evolution of life histories.