Sexual dimorphism in subterranean amphipod crustaceans covaries with subterranean habitat type.

Sexual dimorphism can evolve in response to sex-specific selection pressures that vary across habitats. We studied sexual differences in subterranean amphipods Niphargus living in shallow subterranean habitats (close to the surface), cave streams (intermediate), and cave lakes (deepest and most isolated). These three habitats differ because at greater depths there is lower food availability, reduced predation, and weaker seasonality. Additionally, species near the surface have a near-even adult sex ratio (ASR), whereas species from cave lakes have a female-biased ASR. We hypothesized (a) a decrease in sexual dimorphism from shallow subterranean habitats to cave lake species because of weaker sexual selection derived from changes in the ASR and (b) an increase in female body size in cave lakes because of stronger fecundity selection on account of oligotrophy, reduced predation, and weaker seasonality. We measured body size and two sexually dimorphic abdominal appendages for all 31 species and several behaviours related to male competition (activity, risk-taking, exploration) for 12 species. Species with an equal ASR that live close to the surface exhibited sexual dimorphism in all three morphological traits, but not in behaviour. The body size of females increased from the surface to cave lakes, but no such trend was observed in males. In cave lake species, males and females differed neither morphologically nor behaviourally. Our results are consistent with the possibility that sexual and fecundity selection covary across the three habitats, which indirectly and directly, respectively, shape the degree of sexual dimorphism in Niphargus species.

Fitness as the organismal performance measure guiding adaptive evolution.

A long-standing problem in evolutionary theory is to clarify in what sense (if any) natural selection cumulatively improves the design of organisms. Various concepts, such as fitness and inclusive fitness, have been proposed to resolve this problem. In addition, there have been attempts to replace the original problem with more tractable questions, such as whether a given gene or trait is favored by selection. Here, we ask what theoretical properties the concept fitness should possess to encapsulate the improvement criterion required to talk meaningfully about adaptive evolution. We argue that natural selection tends to shape phenotypes based on the causal properties of individuals and that this tendency is, therefore, best captured by a fitness concept that focuses on these properties. We highlight a fitness concept that meets this role under broad conditions but requires adjustments in our conceptual understanding of adaptive evolution. These adjustments combine elements of Dawkinsian gene selectionism and Egbert Leigh's "parliament of genes."

A general framework for modelling trade-offs in adaptive behaviour.

An animal's behaviour can influence many variables, such as its energy reserves, its risk of injury or mortality, and its rate of reproduction. To identify the optimal action in a given situation, these various effects can be compared in the common currency of reproductive value. While this idea has been widely used to study trade-offs between pairs of variables, e.g. between energy gain versus survival, here we present a unified framework that makes explicit how these various trade-offs fit together. This unification covers a wide range of biological phenomena, highlighting similarities in their logical structure and helping to identify knowledge gaps. To fill one such gap, we present a new model of foraging under the risk of predation and damage accumulation. We conclude by discussing the use and limitations of state-dependent optimisation theory in predicting biological observations.

Sex roles and sex ratios in animals.

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.

The evolution of mating preferences for genetic attractiveness and quality in the presence of sensory bias.

The aesthetic preferences of potential mates have driven the evolution of a baffling diversity of elaborate ornaments. Which fitness benefit-if any-choosers gain from expressing such preferences is controversial, however. Here, we simulate the evolution of preferences for multiple ornament types (e.g., "Fisherian," "handicap," and "indicator" ornaments) that differ in their associations with genes for attractiveness and other components of fitness. We model the costs of preference expression in a biologically plausible way, which decouples costly mate search from cost-free preferences. Ornaments of all types evolved in our model, but their occurrence was far from random. Females typically preferred ornaments that carried information about a male's quality, defined here as his ability to acquire and metabolize resources. Highly salient ornaments, which key into preexisting perceptual biases, were also more likely to evolve. When males expressed quality-dependent ornaments, females invested readily in costly mate search to locate preferred males. In contrast, the genetic benefits associated with purely arbitrary ornaments were insufficient to sustain highly costly mate search. Arbitrary ornaments could nonetheless "piggyback" on mate-search effort favored by other, quality-dependent ornaments. We further show that the potential to produce attractive male offspring ("sexy sons") can be as important as producing offspring of high general quality ("good genes") in shaping female preferences, even when preferred ornaments are quality dependent. Our model highlights the importance of mate-search effort as a driver of aesthetic coevolution.

Biological adaptation in light of the Lewontin-Williams (a)symmetry.

Neo-Darwinism characterizes biological adaptation as a one-sided process, in which organisms adapt to their environment but not vice versa. This asymmetric relationship-here called Williams' asymmetry-is called into question by Niche Construction Theory, which emphasizes that organisms and their environments often mutually affect each other. Here, we clarify that Williams' asymmetry is specifically concerned with (quasi)-directed modifications toward phenotypes that increase individual fitness. This directedness-which drives the adaptive fit between organism and environment-entails far more than the mere presence of cause-effect relationships. We argue that difficulties with invoking fitness as the guiding principle of adaptive evolution are resolved with an appropriate definition of fitness and that objections against Williams' asymmetry reflect confusions about the nature of biological adaptation.

Size-dependent aggression towards kin in a cannibalistic species.

In juveniles extreme intraspecies aggression can seem counter-intuitive, as it might endanger their developmental goal of surviving until reproductive stage. Ultimately, aggression can be vital for survival, although the factors (e.g., genetic or environmental) leading to the expression and intensity of this behavior vary across taxa. Attacking (and sometimes killing) related individuals may reduce inclusive fitness; as a solution to this problem, some species exhibit kin discrimination and preferentially attack unrelated individuals. Here, we used both experimental and modeling approaches to consider how physical traits (e.g., size in relation to opponent) and genetic relatedness mediate aggression in dyads of cannibalistic Dendrobates tinctorius tadpoles. We paired full-sibling, half-sibling, and non-sibling tadpoles of different sizes together in an arena and recorded their aggression and activity. We found that the interaction between relative size and relatedness predicts aggressive behavior: large individuals in non-sibling dyads are significantly more aggressive than large individuals in sibling dyads. Unexpectedly, although siblings tended to attack less overall, in size-mismatched pairs they attacked faster than in non-sibling treatments. Using a theoretical model to complement these empirical findings, we propose that larval aggression reflects a balance between relatedness and size where individuals trade-off their own fitness with that of their relatives. Lay SummaryBefore you eat someone, you have to attack them first. Here, we investigated the factors that shape aggression in the cannibalistic tadpoles of the dyeing poison frog. We find that aggression depends on both size and relatedness: when set in pairs, large tadpoles are half as aggressive towards their smaller siblings than to nonsibs. It looks like belonging to the same family provides some protection against aggression, though no one is ever truly safe.

The balance model of honest sexual signaling.

Costly signaling theory is based on the idea that individuals may signal their quality to potential mates and that the signal's costliness plays a crucial role in maintaining information content ("honesty") over evolutionary time. Although costly signals have traditionally been described as "handicaps," here we present mathematical results that motivate an alternative interpretation. We show that under broad conditions, the multiplicative nature of fitness selects for roughly balanced investments in mating success and viability, thereby generating a positive correlation between signal size and quality. This balancing tendency occurs because selection for increased investment in a fitness component diminishes with the absolute level of investment in that component, such that excessively biased investments are penalized. The resulting interpretation of costly signals as balanced (albeit not necessarily equal) investments may be a widely applicable alternative to the traditional "handicap" metaphor, which has been criticized for its non-Darwinian connotation of selection for "waste" rather than efficiency. We predict that accelerating returns on viability are necessary to undermine honesty. This prediction depends crucially on the assumption that mating success and viability contribute multiplicatively (rather than additively) to an individual's fitness.

Should dispersers be fast learners? Modeling the role of cognition in dispersal syndromes.

Both cognitive abilities and dispersal tendencies can vary strongly between individuals. Since cognitive abilities may help dealing with unknown circumstances, it is conceivable that dispersers may rely more heavily on learning abilities than residents. However, cognitive abilities are costly and leaving a familiar place might result in losing the advantage of having learned to deal with local conditions. Thus, individuals which invested in learning to cope with local conditions may be better off staying at their natal place. In order to disentangle the complex relationship between dispersal and learning abilities, we implemented individual-based simulations. By allowing for developmental plasticity, individuals could either become a 'resident' or 'dispersal' cognitive phenotype. The model showed that in general residents have higher learning abilities than dispersers. Dispersers evolve higher learning ability than residents when dispersers have long life spans and when dispersal occurs either early or late in life, thereby maximizing the time in one habitat patch. Time is crucial here, because the longer an individual resides in a location where it can use its learned knowledge or behavior, the more often it profits from it and thus eventually obtains a net benefit from its investment into learning. Both, longevity and the timing of dispersal within lifecycles determine the time individuals have to recoup that investment and thus crucially influence this correlation. We therefore suggest that species' life history will strongly impact the expected cognitive abilities of dispersers, relative to their resident conspecifics, and that cognitive abilities might be an integral part of dispersal syndromes.

No room for males in caves: Female-biased sex ratio in subterranean amphipods of the genus Niphargus.

Sex allocation theory predicts that the proportion of daughters to sons will evolve in response to ecological conditions that determine the costs and benefits of producing each sex. All else being equal, the adult sex ratio (ASR) should also vary with ecological conditions. Many studies of subterranean species reported female-biased ASR, but no systematic study has yet been conducted. We test the hypothesis that the ASR becomes more female-biased with increased isolation from the surface. We compiled a data set of ASRs of 35 species in the subterranean amphipod Niphargus, each living in one of three distinct habitats (surface-subterranean boundary, cave streams, phreatic lakes) representing an environmental gradient of increased isolation underground. The ASR was female-biased in 27 of 35 species; the bias was statistically significant in 12 species. We found a significant difference in the ASR among habitats after correction for phylogeny. It is most weakly female-biased at the surface-subterranean boundary and most strongly female-biased in phreatic lakes. Additional modelling suggests that the ASR has evolved towards a single value for both surface-subterranean boundary and cave stream-dwelling species, and another value for 9 of 11 phreatic lake dwellers. We suggest that a history of inbreeding in subterranean populations might lower inbreeding depression such that kin selection favours mating with siblings. This could select for a female-biased offspring sex ratio due to local mate competition among brothers. The observed patterns in sex ratios in subterranean species make them a group worthy of more attention from those interested in sex allocation theory.

Realistic genetic architecture enables organismal adaptation as predicted under the folk definition of inclusive fitness.

A fundamental task of evolutionary biology is to explain the pervasive impression of organismal design in nature, including traits benefiting kin. Inclusive fitness is considered by many to be a crucial piece in this puzzle, despite ongoing discussion about its scope and limitations. Here, we use individual-based simulations to study what quantity (if any) individual organisms become adapted to maximize when genetic architectures are more or less suitable for the presumed main driver of biological adaptation, namely cumulative multi-locus evolution. As an expository device, we focus on a hypothetical situation called Charlesworth's paradox, in which altruism is seemingly predicted to evolve, yet altruists immediately perish along with their altruistic genes. Our results support a recently proposed re-definition of inclusive fitness, which is concerned with the adaptive design of whole organisms as shaped by multi-locus evolution, rather than with selection for any focal gene. They also illustrate how our conceptual understanding of adaptation at the phenotypic level should inform our choice of genetic assumptions in abstract simplified models.

Hybridization selects for prime-numbered life cycles in Magicicada: An individual-based simulation model of a structured periodical cicada population.

We investigate competition between separate periodical cicada populations each possessing different life-cycle lengths. We build an individual-based model to simulate the cicada life cycle and allow random migrations to occur between patches inhabited by the different populations. We show that if hybridization between different cycle lengths produces offspring that have an intermediate life-cycle length, then predation acts disproportionately to select against the hybrid offspring. This happens because they emerge in low densities without the safety-in-numbers provided by either parent population. Thus, prime-numbered life cycles that can better avoid hybridization are favored. However, we find that this advantage of prime-numbered cycles occurs only if there is some mechanism that can occasionally synchronize emergence between local populations in sufficiently many patches.

Modelling the evolution of cognitive styles.

BACKGROUND: Individuals consistently differ in behaviour, exhibiting so-called personalities. In many species, individuals differ also in their cognitive abilities. When personalities and cognitive abilities occur in distinct combinations, they can be described as 'cognitive styles'. Both empirical and theoretical investigations produced contradicting or mixed results regarding the complex interplay between cognitive styles and environmental conditions. RESULTS: Here we use individual-based simulations to show that, under just slightly different environmental conditions, different cognitive styles exist and under a variety of conditions, can also co-exist. Co-existences are based on individual specialization on different resources, or, more generally speaking, on individuals adopting different niches or microhabitats. CONCLUSIONS: The results presented here suggest that in many species, individuals of the same population may adopt different cognitive styles. Thereby the present study may help to explain the variety of styles described in previous studies and why different, sometimes contradicting, results have been found under similar conditions.

Need for speed: Short lifespan selects for increased learning ability.

It is generally assumed that an investment into cognitive abilities and their associated cost is particularly beneficial for long-lived species, as a prolonged lifespan allows to recoup the initial investment. However, ephemeral organisms possess astonishing cognitive abilities too. Invertebrates, for example, are capable of simple associative learning, reversal learning, and planning. How can this discrepancy between theory and evidence be explained? Using a simulation, we show that short lives can actually select for an increase in learning abilities. The rationale behind this is that when learning is needed to exploit otherwise inaccessible resources, one needs to learn fast in order to utilize the resources when constrained by short lifespans. And thus, increased cognitive abilities may evolve, not despite short lifespan, but because of it.

Sex roles and the evolution of parental care specialization.

Males and females are defined by the relative size of their gametes (anisogamy), but secondary sexual dimorphism in fertilization, parental investment and mating competition is widespread and often remarkably stable over evolutionary timescales. Recent theory has clarified the causal connections between anisogamy and the most prevalent differences between the sexes, but deviations from these patterns remain poorly understood. Here, we study how sex differences in parental investment and mating competition coevolve with parental care specialization. Parental investment often consists of two or more distinct activities (e.g. provisioning and defence) and parents may care more efficiently by specializing in a subset of these activities. Our model predicts that efficient care specialization broadens the conditions under which biparental investment can evolve in lineages that historically had uniparental care. Major transitions in sex roles (e.g. from female-biased care with strong male mating competition to male-biased care with strong female competition) can arise following ecologically induced changes in the costs or benefits of different care types, or in the sex ratio at maturation. Our model provides a clear evolutionary mechanism for sex-role transitions, but also predicts that such transitions should be rare. It consequently contributes towards explaining widespread phylogenetic inertia in parenting and mating systems.

The strategic reference gene: an organismal theory of inclusive fitness.

How to define and use the concept of inclusive fitness is a contentious topic in evolutionary theory. Inclusive fitness can be used to calculate selection on a focal gene, but it is also applied to whole organisms. Individuals are then predicted to appear designed as if to maximize their inclusive fitness, provided that certain conditions are met (formally when interactions between individuals are 'additive'). Here we argue that applying the concept of inclusive fitness to organisms is justified under far broader conditions than previously shown, but only if it is appropriately defined. Specifically, we propose that organisms should maximize the sum of their offspring ( including any accrued due to the behaviour/phenotype of relatives), plus any effects on their relatives' offspring production, weighted by relatedness. By contrast, most theoreticians have argued that a focal individual's inclusive fitness should exclude any offspring accrued due to the behaviour of relatives. Our approach is based on the notion that long-term evolution follows the genome's 'majority interest' of building coherent bodies that are efficient 'vehicles' for gene propagation. A gene favoured by selection that reduces the propagation of unlinked genes at other loci (e.g. meiotic segregation distorters that lower sperm production) is eventually neutralized by counter-selection throughout the rest of the genome. Most phenotypes will therefore appear as if designed to maximize the propagation of any given gene in a focal individual and its relatives.

Evolutionary Hysteresis and Ratchets in the Evolution of Periodical Cicadas.

It has been previously hypothesized that the perfectly synchronized mass emergence of periodical cicadas (Magicicada spp.) evolved as a result of a switch from size-based to age-based emergence. In the former case, cicada nymphs emerge immediately (at the first opportunity) on reaching maturity, whereas in the latter case, nymphs wait in order to emerge at a specific age. Here we use an individual-based model to simulate the cicada life cycle and to study the evolution of periodicity. We find that if age-based emergence evolves in a constant abiotic environment, it typically results in a population that is protoperiodic, and synchronous emergence of the whole population is not achieved. However, perfect periodicity and synchronous emergence can be attained, if the abiotic environment changes back and forth between favorable and unfavorable conditions (hysteresis). Furthermore, once age-based emergence evolves, generally it can only be invaded by other age-based emergence strategies with longer cycle lengths (evolutionary ratchet). Together, these mechanisms promote the evolution of long periodic life cycles and synchronous emergence in the Magicicada. We discuss how our results connect to previous theories and recent phylogenetic studies on Magicicada evolution.

Sexual selection, phenotypic plasticity and female reproductive output.

In a rapidly changing environment, does sexual selection on males elevate a population's reproductive output? If so, does phenotypic plasticity enhance or diminish any such effect? We outline two routes by which sexual selection can influence the reproductive output of a population: a genetic correlation between male sexual competitiveness and female lifetime reproductive success; and direct effects of males on females' breeding success. We then discuss how phenotypic plasticity of sexually selected male traits and/or female responses (e.g. plasticity in mate choice), as the environment changes, might influence how sexual selection affects a population's reproductive output. Two key points emerge. First, condition-dependent expression of male sexual traits makes it likely that sexual selection increases female fitness if reproductively successful males disproportionately transfer genes that are under natural selection in both sexes, such as genes for foraging efficiency. Condition-dependence is a form of phenotypic plasticity if some of the variation in net resource acquisition and assimilation is attributable to the environment rather than solely genetic in origin. Second, the optimal allocation of resources into different condition-dependent traits depends on their marginal fitness gains. As male condition improves, this can therefore increase or, though rarely highlighted, actually decrease the expression of sexually selected traits. It is therefore crucial to understand how condition determines male allocation of resources to different sexually selected traits that vary in their immediate effects on female reproductive output (e.g. ornaments versus coercive behaviour). In addition, changes in the distribution of condition among males as the environment shifts could reduce phenotypic variance in certain male traits, thereby reducing the strength of sexual selection imposed by females. Studies of adaptive evolution under rapid environmental change should consider the possibility that phenotypic plasticity of sexually selected male traits, even if it elevates male fitness, could have a negative effect on female reproductive output, thereby increasing the risk of population extinction. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Sex-allocation conflict and sexual selection throughout the lifespan of eusocial colonies.

Models of sex-allocation conflict are central to evolutionary biology but have mostly assumed static decisions, where resource allocation strategies are constant over colony lifespan. Here, we develop a model to study how the evolution of dynamic resource allocation strategies is affected by the queen-worker conflict in annual eusocial insects. We demonstrate that the time of dispersal of sexuals affects the sex-allocation ratio through sexual selection on males. Furthermore, our model provides three predictions that depart from established results of classic static allocation models. First, we find that the queen wins the sex-allocation conflict, while the workers determine the maximum colony size and colony productivity. Second, male-biased sex allocation and protandry evolve if sexuals disperse directly after eclosion. Third, when workers are more related to new queens, then the proportional investment into queens is expected to be lower, which results from the interacting effect of sexual selection (selecting for protandry) and sex-allocation conflict (selecting for earlier switch to producing sexuals). Overall, we find that colony ontogeny crucially affects the outcome of sex-allocation conflict because of the evolution of distinct colony growth phases, which decouples how queens and workers affect allocation decisions and can result in asymmetric control.

Not all sex ratios are equal: the Fisher condition, parental care and sexual selection.

The term 'sex roles' encapsulates male-female differences in mate searching, competitive traits that increase mating/fertilization opportunities, choosiness about mates and parental care. Theoretical models suggest that biased sex ratios drive the evolution of sex roles. To model sex role evolution, it is essential to note that in most sexually reproducing species (haplodiploid insects are an exception), each offspring has one father and one mother. Consequently, the total number of offspring produced by each sex is identical, so the mean number of offspring produced by individuals of each sex depends on the sex ratio (Fisher condition). Similarly, the total number of heterosexual matings is identical for each sex. On average, neither sex can mate nor breed more often when the sex ratio is even. But equally common in which sex ratio? The Fisher condition only applies to some reproductive measures (e.g. lifetime offspring production or matings) for certain sex ratios (e.g. operational or adult sex ratio; OSR, ASR). Here, we review recent models that clarify whether a biased OSR, ASR or sex ratio at maturation (MSR) have a causal or correlational relationship with the evolution of sex differences in parental care and competitive traits-two key components of sex roles. We suggest that it is more fruitful to understand the combined effect of the MSR and mortality rates while caring and competing than that of the ASR itself. In short, we argue that the ASR does not have a causal role in the evolution of parental care. We point out, however, that the ASR can be a cue for adaptive phenotypic plasticity in how each sex invests in parental care.This article is part of the themed issue 'Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies'.