0000000001305168
AUTHOR
Hanna Kokko
How partnerships end in guillemots Uria aalge : chance events, adaptive change, or forced divorce?
Divorce in socially monogamous species can result from different mechanisms, for example, chance events, active desertion of the partner, or the intrusion of a third individual ousting the partner. We compared the predictions associated with such mechanisms with data from common guillemots (Uria aalge) breeding on the Isle of May, Scotland. The data cover the years 1982--2005 and show a yearly divorce rate of 10.2%. In most divorces (86%), one of the original partners moved to another breeding site, whereas the other bird stayed and bred with a new partner. On average, movers had a significantly lower breeding success after divorce, stayers were largely unaffected, whereas the incoming bird…
It takes two to tango
Abstract In most taxa, females are more likely than males to care for offspring. Why? Ever since Trivers' landmark work, the answer has been traced back to sexual differences in pre-mating reproductive investment (unequal gamete size or anisogamy). However, recent work shows that parental investment theory has inadvertently ignored a profoundly simple fact of life: every offspring has a mother and father. Taking this into account completely changes how we should think about sex differences in parental care.
Stepping stones of life: natal dispersal in the group-living but noncooperative speckled warbler
In most cooperatively breeding birds the offspring of one sex, usually male, delays dispersal to remain on the natal territory and helps its parents to rear subsequent young. Thus delayed dispersal could be the first step in the evolution of cooperative breeding. We studied natal dispersal in a population of the group-living speckled warbler, Chthonicola sagittata, based on observations of a colour-banded population over 3 years. Unlike other group-living members of the Acanthizinae, all juvenile males in this population dispersed to settle on foreign territories as subordinates, which do not help rear the young. Speckled warblers showed all the life history traits that are thought to resul…
Priority versus Brute Force: When Should Males Begin Guarding Resources?
When should males begin guarding a resource when both resources and guarders vary in quality? This general problem applies, for example, to migrant birds occupying territories in the spring and to precopula in crustaceans where males grab females before they molt and become receptive. Previous work has produced conflicting predictions. Theory on migrant birds predicts that the strongest competitors should often arrive first, whereas some models of mate guarding have predicted that the strongest competitors wait and then simply usurp a female from a weaker competitor. We build a general model of resource guarding that allows varying the ease with which takeovers occur. The model is phrased i…
Daphnia females adjust sex allocation in response to current sex ratio and density
Cyclical parthenogenesis presents an interesting challenge for the study of sex allocation, as individuals’ allocation decisions involve both the choice between sexual and asexual reproduction, and the choice between sons and daughters. Male production is therefore expected to depend on ecological and evolutionary drivers of overall investment in sex, and those influencing male reproductive value during sexual periods. We manipulated experimental populations, and made repeated observations of natural populations over their growing season, to disentangle effects of population density and the timing of sex from effects of adult sex ratio on sex allocation in cyclically parthenogenetic Daphnia…
Quantifying male attractiveness
Genetic models of sexual selection are concerned with a dynamic process in which female preference and male trait values coevolve. We present a rigorous method for characterizing evolutionary endpoints of this process in phenotypic terms. In our phenotypic characterization the mate-choice strategy of female population members determines how attractive females should find each male, and a population is evolutionarily stable if population members are actually behaving in this way. This provides a justification of phenotypic explanations of sexual selection and the insights into sexual selection that they provide. Furthermore, the phenotypic approach also has enormous advantages over a genetic…
Figure S1;Figure S2 from Daphnia invest in sexual reproduction when its relative costs are reduced
Figure S1. Occurrence of sexually reproducing females in the population with respect to asexual reproductive effort. Grey lines show the logistic regression within populations, whereas the pink line shows the logistic regression across populations. The inflection point (black line) indicates the threshold mean asexual reproductive effort (e2.44=11.47) at which the majority of populations contain females that carry a sexual clutch. Light grey dots show the raw data.;Figure S2. Temporal dynamics (day 1 = May 30, 2015) of (a) population density (Daphnia/L), (b) asexual reproductive effort, (c) population growth rate, and (d) the proportion of sexual females in the population. Each line shows o…
Reproductive timing and individual fitness
Estimation of individual fitness – i.e. description of the extent to which an individual's genes are represented in future generations – is a feature central to most evolutionary studies. Lifetime reproductive success (LRS) is a commonly used estimate of individual fitness, but because it is rate-insensitive (i.e. timing of reproductive events is not incorporated), it may give a biased estimate of fitness when reproductive timing is an important component of fitness. A review of all empirical studies which have used a recently derived, rate-sensitive estimate of individual fitness, λind revealed that λind ranks the fitness of phenotypes differently from LRS, and that this difference may lea…
The evolution of sex roles in mate searching
Searching for mates is a critical stage in the life cycle of most internally, and many externally, fertilizing species. Males usually invest more in this costly activity than females, but the reasons for this are poorly understood. Previous models have shown that female-biased parental investment, including anisogamy, does not by itself select for male-biased mate searching, so it requires additional explanations. Here, we correct and expand upon earlier models, and present two novel hypotheses that might explain the evolution of male-biased mate searching. The "carry-over hypothesis" states that females benefit less from searching if the associated costs affect other stages of the life cyc…
Territorial defense, territory size, and population regulation.
The carrying capacity of an environment is determined partly by how individuals compete over the available resources. To territorial animals, space is an important resource, leading to conflict over its use. We build a model where the carrying capacity for an organism in a given environment results from the evolution of territorial defense effort and the consequent space use. The same evolutionary process can yield two completely different modes of population regulation. Density dependence arises through expanding and shrinking territories if fecundity is low, breeding success increases gradually with territory size, and/or defense is cheap. By contrast, when fecundity is high, breeding suc…
Daphnia invest in sexual reproduction when its relative costs are reduced
The timing of sex in facultatively sexual organisms is critical to fitness, due to the differing demographic consequences of sexual versus asexual reproduction. In addition to the costs of sex itself, an association of sex with the production of dormant life stages also influences the optimal use of sex, especially in environments where resting eggs are essential to survive unfavourable conditions. Here we document population dynamics and the occurrence of sexual reproduction in natural populations of Daphnia magna across their growing season. The frequency of sexually reproducing females and males increased with population density and with decreasing asexual clutch sizes. The frequency of…
Seasonal changes in predator community switch the direction of selection for prey defences
Insect communities consist of aposematic species with efficient warning colours against predation, as well as abundant examples of crypsis. To understand such coexistence, we here report results from a field experiment where relative survival of artificial larvae, varying in conspicuousness, was estimated in natural bird communities over an entire season. This takes advantage of natural variation in the proportion of naive predators: naivety peaks when young birds have just fledged. We show that the relative benefit of warning signals and crypsis changes accordingly. When naive birds are rare (early and late in the season), conspicuous warning signals improve survival, but conspicuousness b…
Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus.
Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show …
Sex Allocation Theory for Facultatively Sexual Organisms Inhabiting Seasonal Environments: The Importance of Bet Hedging
Adaptive explanations for dormancy often invoke bet hedging, where reduced mean fitness can be adaptive if it associates with reduced fitness variance. Sex allocation theory typically ignores variance effects and focuses on mean fitness. For many cyclical parthenogens, these themes become linked, as only sexually produced eggs undergo the dormancy needed to survive harsh conditions. We ask how sex allocation and the timing of sex evolve when this constraint exists in the form of a trade-off between asexual reproduction and sexual production of dormant eggs-the former being crucial for within-season success and the latter for survival across seasons. We show that male production can be tempo…
Identification of five novel tectiviruses in Bacillus strains: analysis of a highly variable region generating genetic diversity
Our biosphere is abundant with unique and small genes for which no homologs are known. These genes, often referred to as orphans or ORFans, are commonly found in bacteriophage genomes but their origins remain unclear. We discovered five novel tectivirus-like genetic elements by screening more than five-hundred Bacillus strains. A highly variable region (HVR) of these viruses was shown to harbor ORFans in most of these otherwise well-conserved bacteriophages. Previous studies demonstrated that mutations close to this region dramatically alter bacteriophage gene regulation, suggesting that the acquisition of those ORFans may provide a source of genetic diversity that is then subject to geneti…
Sex ratio and sexual conflict in a collective action problem
AbstractThe maintenance of cooperation is difficult whenever collective action problems are vulnerable to freeriding (reaping the benefits without contributing to the maintenance of the good). We identify a novel factor that can make a system tolerate an extent of freeriding. If a population consists of discrete types with demographically distinct roles, such that the success of one type does not imply it can spread to replace other types in the population, then collective goods may persist in the presence of free-riders because they are necessarily kept in a minority role. Biased sex ratios (e.g. in haplodiploids) create conditions where individuals of one sex are a minority. We show that …
Multiple mating by females is a natural outcome of a null model of mate encounters
Why do females of so many species mate multiply? The question makes use of an implicit null model that females by default should be monandrous and that polyandry requires an explanation. Here, we make thesimplepoint that females encountermates overtheir lifetimeina stochasticmanner,andas theyshouldacceptatleastonemale,acceptanceofallmales maybea betternullmodelthanthemore advanced strategy of accepting thefirst satisfactory one and rejecting all others. The advantage of this view is that it makes it explicit that females must accept and reject mates without precise knowledge of future mate encounters. In insects, for example, limitations of cognitive and sensory capabilities make it hard fo…
From arctic lemmings to adaptive dynamics: Charles Elton's legacy in population ecology.
We shall examine the impact of Charles S. Elton's 1924 article on periodic fluctuations in animal populations on the development of modern population ecology. We argue that his impact has been substantial and that during the past 75 years of research on multi-annual periodic fluctuations in numbers of voles, lemmings, hares, lynx and game animals he has contributed much to the contemporary understanding of the causes and consequences of population regulation. Elton was convinced that the cause of the regular fluctuations was climatic variation. To support this conclusion, he examined long-term population data then available. Despite his firm belief in a climatic cause of the self-repeating …
Evolutionary conservation advice for despotic populations: habitat heterogeneity favours conflict and reduces productivity in Seychelles magpie robins
Individual preferences for good habitat are often thought to have a beneficial stabilizing effect for populations. However, if individuals preferentially compete for better-quality territories, these may become hotspots of conflict. We show that, in an endangered species, this process decreases the productivity of favoured territories to the extent that differences in productivity between territories disappear. Unlike predictions from current demographic theory on site-dependent population regulation (ideal despotic distribution), we show that population productivity is reduced if resources are distributed unevenly in space. Competition for high-quality habitat can thus have detrimental con…
Adaptive strategies of territory formation
How do territorial animals gain ownership of an area? Early modelling has considered the evolution of fighting when the winner can claim the right to the resource. Recently, alternative hypotheses have been offered where repeated interactions lead to division of space through 'nagging' instead of one decisive fight. However, these models assume that animals avoid areas in which they have taken part in aggressive interactions, but do not consider whether avoidance itself is adaptive. We aim to bridge this gap between mechanistic and adaptive explanations, by presenting a game-theory model where individuals choose whether to return to an area after a fight with a specific outcome (win, loss, …
Species-level selection reduces selfishness through competitive exclusion.
Adaptation does not necessarily lead to traits which are optimal for the population. This is because selection is often the strongest at the individual or gene level. The evolution of selfishness can lead to a ‘tragedy of the commons’, where traits such as aggression or social cheating reduce population size and may lead to extinction. This suggests that species-level selection will result whenever species differ in the incentive to be selfish. We explore this idea in a simple model that combines individual-level selection with ecology in two interacting species. Our model is not influenced by kin or trait-group selection. We find that individual selection in combination with competitive ex…
Social transmission of avoidance among predators facilitates the spread of novel prey.
Warning signals are an effective defence strategy for aposematic prey, but only if they are recognized by potential predators. If predators must eat prey to associate novel warning signals with unpalatability, how can aposematic prey ever evolve? Using experiments with great tits (Parus major) as predators, we show that social transmission enhances the acquisition of avoidance by a predator population. Observing another predator’s disgust towards tasting one novel conspicuous prey item led to fewer aposematic than cryptic prey being eaten for the predator population to learn. Despite reduced personal encounters with unpalatable prey, avoidance persisted and increased over subsequent trials.…
Competition for breeding sites and site-dependent population regulation in a highly colonial seabird, the common guillemot Uria aalge
Summary 1. The hypothesis of site-dependent population regulation predicts that birds utilize available nesting sites in a pre-emptive (ideal despotic) manner, leading to density dependence in heterogeneous habitats as poorer sites are used at higher population densities. At small population sizes adaptive site choice protects populations against fluctuations (the buffer effect). 2. Common guillemots Uria aalge (Pontoppidan) breed at high density on sea-cliffs. The population breeding on the Isle of May, Scotland increased by 60% between 1981 and 2000. A good nest-site is a prerequisite for successful breeding and there is much competition for the best sites. Throughout this period, site us…
Population-level consequences of risky dispersal
Achieving sufficient connectivity between populations is essential for persistence, but costs of dispersal may select against individual traits or behaviours that, if present, would improve connectivity. Existing dispersal models tend to ignore the multitude of risks to individuals: while many assess the effect of mortality costs, there is also a risk of failing to find new habitat, especially when the entire inhabitable area remains both small and fragmented. There are few known rules governing whether individuals evolve to disperse more, or less, than what is ideal for population connectivity and persistence. Here we aim to fill this gap, while also noting that evolution might not only pr…
Sex Allocation Theory for Facultatively Sexual Organisms Inhabiting Seasonal Environments: The Importance of Bet Hedging
Adaptive explanations for dormancy often invoke bet hedging, where reduced mean fitness can be adaptive if it associates with reduced fitness variance. Sex allocation theory typically ignores variance effects and focuses on mean fitness. For many cyclical parthenogens, these themes become linked, as only sexually produced eggs undergo the dormancy needed to survive harsh conditions. We ask how sex allocation and the timing of sex evolve when this constraint exists in the form of a trade-off between asexual reproduction and sexual production of dormant eggs—the former being crucial for within-season success and the latter for survival across seasons. We show that male production can be tempo…
SEXUALLY SELECTED TRAITS EVOLVE POSITIVE ALLOMETRY WHEN SOME MATINGS OCCUR IRRESPECTIVE OF THE TRAIT
Positive allometry of secondary sexual traits (whereby larger individuals have disproportionally larger traits than smaller individuals) has been called one of the most pervasive and poorly understood regularities in the study of animal form and function. Its widespread occurrence is in contrast with theoretical predictions that it should evolve only under rather special circumstances. Using a combination of mathematical modeling and simulations, here we show that positive allometry is predicted to evolve under much broader conditions than previously recognized. This result hinges on the assumption that mating success is not necessarily zero for males with the lowest trait values: for examp…
Debating Sexual Selection and Mating Strategies
Published at full length with the title 'Reproductive behaviour: sexual selection remains the best explanation' in Science E-letters, 6 April 2006
SEXUAL SELECTION WHEN FERTILIZATION IS NOT GUARANTEED
Much of the theory of sexual selection assumes that females do not generally experience difficulties getting their eggs fertilized, yet sperm limitation is occasionally documented. How often does male limitation form a selection for female traits that improve their mating rate? The question is difficult to test, because if such traits evolve to be efficient, sperm limitation will no longer appear to be a problem to females. Here, we suggest that changes in choosiness between populations, and in particular between virgin and mated females, offer an efficient way to test this hypothesis. We model the "wallflower effect," that is, changes in female preferences due to time and mortality costs o…
Sexually selected traits evolve positive allometry when some matings occur irrespective of the trait
Positive allometry of secondary sexual traits (whereby larger individuals have disproportionally larger traits than smaller individuals) has been called one of the most pervasive and poorly understood regularities in the study of animal form and function. Its widespread occurrence is in contrast with theoretical predictions that it should evolve only under rather special circumstances. Using a combination of mathematical modeling and simulations, here we show that positive allometry is predicted to evolve under much broader conditions than previously recognized. This result hinges on the assumption that mating success is not necessarily zero for males with the lowest trait values: for examp…
Colour polymorphism torn apart by opposing positive frequency-dependent selection, yet maintained in space.
Summary Polymorphic warning signals in aposematic species are enigmatic because predator learning and discrimination should select for the most common coloration, resulting in positive frequency‐dependent survival selection. Here, we investigated whether differential mating success could create sufficiently strong negative frequency‐dependent selection for rare morphs to explain polymorphic (white and yellow) warning coloration in male wood tiger moths (Parasemia plantaginis). We conducted an experiment in semi‐natural conditions where we estimated mating success for both white and yellow male moths under three different morph frequencies. Contrary to expectations, mating success was positi…
Dynamics of the caring family
When several individuals simultaneously provide for offspring, as in families, the effort of any one individual will depend on the efforts of the other family members. This conflict of interest among family members is made more complicated by their relatedness because relatives share genetic interest to some degree. The conflict resolution will also be influenced by the differences in reproductive value between breeders and helpers. Here, we calculate evolutionarily stable provisioning efforts in families with up to two helpers. We explicitly consider that the behavioral choices are made in a life-history context, and we also consider how group sizes change dynamically; this affects, for ex…
From individual dispersal to species ranges: perspectives for a changing world.
Dispersal is often risky to the individual, yet the long-term survival of populations depends on having a sufficient number of individuals that move, find each other, and locate suitable breeding habitats. This tension has consequences that rarely meet our conservation or management goals. This is particularly true in changing environments, which makes the study of dispersal urgently topical in a world plagued with habitat loss, climate change, and species introductions. Despite the difficulty of tracking mobile individuals over potentially vast ranges, recent research has revealed a multitude of ways in which dispersal evolution can either constrain, or accelerate, species' responses to en…
The ecogenetic link between demography and evolution: can we bridge the gap between theory and data?
Calls to understand the links between ecology and evolution have been common for decades. Population dynamics, i.e. the demographic changes in populations, arise from life history decisions of individuals and thus are a product of selection, and selection, on the contrary, can be modified by such dynamical properties of the population as density and stability. It follows that generating predictions and testing them correctly requires considering this ecogenetic feedback loop whenever traits have demographic consequences, mediated via density dependence (or frequency dependence). This is not an easy challenge, and arguably theory has advanced at a greater pace than empirical research. Howeve…
Reproductive conflict delays the recovery of an endangered social species
1. Evolutionary theory predicts that individuals, in order to increase their relative fitness, can evolve behaviours that are detrimental for the group or population. This mismatch is particularly visible in social organisms. Despite its potential to affect the population dynamics of social animals, this principle has not yet been applied to real-life conservation. 2. Social group structure has been argued to stabilize population dynamics due to the buffering effects of nonreproducing subordinates. However, competition for breeding positions in such species can also interfere with the reproduction of breeding pairs. 3. Seychelles magpie robins, Copsychus sechellarum, live in social groups w…
Review Paper: Are reproductive skew models evolutionarily stable?
Reproductive skew theory has become a popular way to phrase problems and test hypotheses of social evolution. The diversity of reproductive skew models probably stems from the ease of generating new variations. However, I show that the logical basis of skew models, that is, the way in which group formation is modelled, makes use of hidden assumptions that may be problematical as they are unlikely to be fulfilled in all social systems. I illustrate these problems by re-analysing the basic concessive skew model with staying incentives. First, the model assumes that dispersal is an all-or-nothing response: all subordinates disperse as soon as concessions drop below a certain value. This leads …
Alternative prey can change model-mimic dynamics between parasitism and mutualism
Classical (conventional) Mullerian mimicry theory predicts that two (or more) defended prey sharing the same signal always benefit each other despite the fact that one species can be more toxic than the other. The quasi-Batesian (unconventional) mimicry theory, instead, predicts that the less defended partner of the mimetic relationship may act as a parasite of the signal, causing a fitness loss to the model. Here we clarify the conditions for parasitic or mutualistic relationships between aposematic prey, and build a model to examine the hypothesis that the availability of alternative prey is crucial to Mullerian and quasi-Batesian mimicry. Our model is based on optimal behaviour of the pr…
Data from: Colour polymorphism torn apart by opposing positive frequency-dependent selection, yet maintained in space
1. Polymorphic warning signals in aposematic species are enigmatic because predator learning and discrimination should select for the most common coloration, resulting in positive frequency-dependent survival selection. 2. Here, we investigated whether differential mating success could create sufficiently strong negative frequency-dependent selection for rare morphs to explain polymorphic (white and yellow) warning coloration in male wood tiger moths (Parasemia plantaginis). 3. We conducted an experiment in semi-natural conditions where we estimated mating success for both white and yellow male moths under three different morph frequencies. 4. Contrary to expectations, mating success was po…
Data from: Sex allocation theory for facultatively sexual organisms inhabiting seasonal environments: the importance of bet-hedging
Adaptive explanations for dormancy often invoke bet-hedging, where reduced mean fitness can be adaptive if it associates with reduced fitness variance. Sex allocation theory typically ignores variance effects and focuses on mean fitness. For many cyclical parthenogens, these themes become linked, as only sexually produced eggs undergo dormancy needed to survive harsh conditions. We ask how sex allocation and the timing of sex evolve when this constraint exists in the form of a trade-off between asexual reproduction and sexual production of dormant eggs — the former being crucial for within-season success, the latter for survival across seasons. We show that male production can be temporally…
Data from: Population-level consequences of risky dispersal
Achieving sufficient connectivity between populations is essential for persistence, but costs of dispersal may select against individual traits or behaviours that, if present, would improve connectivity. Existing dispersal models tend to ignore the multitude of risks to individuals: while many assess the effect of mortality costs, there is also a risk of failing to find new habitat, especially when the entire inhabitable area remains both small and fragmented. There are few known rules governing whether individuals evolve to disperse more, or less, than what is ideal for population connectivity and persistence. Here we aim to fill this gap, while also noting that evolution might not only pr…
Data from: Daphnia females adjust sex allocation in response to current sex ratio and density
Cyclical parthenogenesis presents an interesting challenge for the study of sex allocation, as individuals’ allocation decisions involve both the choice between sexual and asexual reproduction, and the choice between sons and daughters. Male production is therefore expected to depend on ecological and evolutionary drivers of overall investment in sex, and those influencing male reproductive value during sexual periods. We manipulated experimental populations, and made repeated observations of natural populations over their growing season, to disentangle effects of population density and the timing of sex from effects of adult sex ratio on sex allocation in cyclically parthenogenetic Daphnia…
Data from: Daphnia invest in sexual reproduction when its relative costs are reduced
The timing of sex in facultatively sexual organisms is critical to fitness, due to the differing demographic consequences of sexual vs. asexual reproduction. In addition to the costs of sex itself, an association of sex with the production of dormant life stages also influences the optimal use of sex, especially in environments where resting eggs are essential to survive unfavourable conditions. Here we document population dynamics and the occurrence of sexual reproduction in natural populations of Daphnia magna across their growing season. The frequency of sexually reproducing females and males increased with population density and with decreasing asexual clutch sizes. The frequency of sex…
Data from: Negative frequency-dependent selection of sexually antagonistic alleles in Myodes glareolus
Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show …
Data from: Sexually selected traits evolve positive allometry when some matings occur irrespective of the trait
Positive allometry of secondary sexual traits (whereby larger individuals have disproportionally larger traits than smaller individuals) has been called one of the most pervasive and poorly understood regularities in the study of animal form and function. Its widespread occurrence is in contrast with theoretical predictions that it should evolve only under rather special circumstances.