FEATURE THEORY AND THE TWO‐STEP HYPOTHESIS OF MÜLLERIAN MIMICRY EVOLUTION

The two‐step hypothesis of Müllerian mimicry evolution states that mimicry starts with a major mutational leap between adaptive peaks, followed by gradual fine‐tuning. The hypothesis was suggested to solve the problem of apostatic selection producing a valley between adaptive peaks, and appears reasonable for a one‐dimensional phenotype. Extending the hypothesis to the realistic scenario of multidimensional phenotypes controlled by multiple genetic loci can be problematic, because it is unlikely that major mutational leaps occur simultaneously in several traits. Here we consider the implications of predator psychology on the evolutionary process. According to feature theory, single prey traits may be used by predators as features to classify prey into discrete categories. A mutational leap in such a trait could initiate mimicry evolution. We conducted individual‐based evolutionary simulations in which virtual predators both categorize prey according to features and generalize over total appearances. We found that an initial mutational leap toward feature similarity in one dimension facilitates mimicry evolution of multidimensional traits. We suggest that feature‐based predator categorization together with predator generalization over total appearances solves the problem of applying the two‐step hypothesis to complex phenotypes, and provides a basis for a theory of the evolution of mimicry rings.     

Müllerian mimicry: an examination of Fisher's theory of gradual evolutionary change

In 1927, Fisher suggested that Müllerian mimicry evolution could be gradual and driven by predator generalization. A competing possibility is the so-called two-step hypothesis, entailing that Müllerian mimicry evolves through major mutational leaps of a less-protected species towards a better-protected, which sets the stage for coevolutionary fine-tuning of mimicry. At present, this hypothesis seems to be more widely accepted than Fisher's suggestion. We conducted individual-based simulations of communities with predators and two prey types to assess the possibility of Fisher's process leading to a common prey appearance. We found that Fisher's process worked for initially relatively similar appearances. Moreover, by introducing a predator spectrum consisting of several predator types with different ranges of generalization, we found that gradual evolution towards mimicry occurred also for large initial differences in prey appearance. We suggest that Fisher's process together with a predator spectrum is a realistic alternative to the two-step hypothesis and, furthermore, it has fewer problems with purifying selection. We also examined the factors influencing gradual evolution towards mimicry and found that not only the relative benefits from mimicry but also the mutational schemes of the prey types matter.     

Calls,colours, shape,and genes: a multi‐trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis

Evolutionary divergence in behavioural traits related to mating may represent the initial stage of speciation. Direct selective forces are usually invoked to explain divergence in mate‐recognition traits, often neglecting a role for neutral processes or concomitant differentiation in ecological traits. We adopted a multi‐trait approach to obtain a deeper understanding of the mechanisms behind allopatric divergence in the Amazonian frog, Allobates femoralis. We tested the null hypothesis that geographic distance between populations correlates with genetic and phenotypic divergence, and compared divergence between mate‐recognition (acoustic) and ecological (coloration, body‐shape) traits. We quantified geographic variation in 39 phenotypic traits and a mitochondrial DNA marker among 125 individuals representing eight populations. Geographic variation in acoustic traits was pronounced and tracked the spatial genetic variation, which appeared to be neutral. Thus, the evolution of acoustic traits tracked the shared history of the populations, which is unexpected for pan‐Amazonian taxa or for mate‐recognition traits. Divergence in coloration appeared uncorrelated with genetic distance, and might be partly attributed to local selective pressures, and perhaps to Batesian mimicry. Divergence in body‐shape traits was low. The results obtained depict a complex evolutionary scenario and emphasize the importance of considering multiple traits when disentangling the forces behind allopatric divergence. ©2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 826–838.     

Do unprofitable prey evolve traits that profitable prey find difficult to exploit?

Prey that are unprofitable to attack (for example, those containing noxious chemicals) are often conspicuously patterned and move in a slower and more predictable manner than species lacking these defences. Contemporary theories suggest these traits have evolved as warning signals because they can facilitate both associative and discriminative avoidance learning in predators. However, it is unclear why these particular traits and not others have tended to evolve in unprofitable prey. Here we show using a signal detection model that unprofitable prey will evolve conspicuous colours and patterns partly because these characteristics cannot readily evolve in profitable prey without close mimicry. The stability of this signal is maintained through the costs of dishonesty in profitable prey. Indeed, unprofitable prey will sometimes evolve a conspicuous form to reduce mimetic parasitism, even in the unlikely event that this form can be more closely mimicked. This is one of the first mathematical models of the evolution of warning signals to allow for the possibility of mimicry, yet our analyses suggest it may offer a general explanation as to why warning signals take the form that they do. Warning signals and mimicry may therefore be more closely related than is currently supposed.     

Genetics of body shape and armour variation in threespine sticklebacks

Patterns of genetic variation and covariation can influence the rate and direction of phenotypic evolution. We explored the possibility that the parallel morphological evolution seen in threespine stickleback (Gasterosteus aculeatus) populations colonizing freshwater environments is facilitated by patterns of genetic variation and covariation in the ancestral (marine) population. We estimated the genetic (G) and phenotypic (P) covariance matrices and directions of maximum additive genetic (g(max) ) and phenotypic (p(max) ) covariances of body shape and armour traits. Our results suggest a role for the ancestral G in explaining parallel morphological evolution in freshwater populations. We also found evidence of genetic constraints owing to the lack of variance in the ancestral G. Furthermore, strong genetic covariances and correlations among traits revealed that selective factors responsible for threespine stickleback body shape and armour divergence may be difficult to disentangle. The directions of g(max) and p(max) were correlated, but the correlations were not high enough to imply that phenotypic patterns of trait variation and covariation within populations are very informative of underlying genetic patterns.     

Warning signals evolve to disengage Batesian mimics

Prey that are unprofitable to attack are typically conspicuous in appearance. Conventional theory assumes that these warning signals have evolved in response to predator receiver biases. However, such biases might be a symptom rather than a cause of warning signals. We therefore examine an alternative theory: that conspicuousness evolves in unprofitable prey to avoid confusion with profitable prey. One might wonder why unprofitable prey do not find a cryptic means to be distinct from profitable prey, reducing both their risk of confusion with profitable prey and their rate of detection by predators. Here we present the first coevolutionary model to allow for Batesian mimicry and signals with different levels of detectability. We find that unprofitable prey do indeed evolve ways of distinguishing themselves using cryptic signals, particularly when appearance traits can evolve in multiple dimensions. However, conspicuous warning signals readily evolve in unprofitable prey when there are more ways to look different from the background than to match it. Moreover, the more unprofitable the prey species, the higher its evolved conspicuousness. Our results provide strong support for the argument that unprofitable species evolve conspicuous signals to avoid confusion with profitable prey and indicate that peak shift in conspicuousness-linked traits is a major factor in its establishment.     

Population differentiation in the swordtail characin (Corynopoma riisei ): a role for sensory drive?

Sensory drive, where the efficacy of a sexual signal depends on the environment in which it is employed, is a potential mechanism behind divergent evolution of secondary sexual traits. Male swordtail characins are equipped with a narrow and transparent extension of the gill cover with a flag‐like structure at its tip. This opercular flag mimics a prey item and is employed by males as a ‘lure’ to attract the attention of females during mating attempts. We conducted a study of genetic and morphological differentiation across swordtail characin populations throughout their native range in Trinidad. The morphology of the opercular flag varied across populations and several aspects of this variation match the predicted hallmarks of sensory drive. First, morphological differentiation of the flag across populations was unrelated to genetic similarity at neutral genetic markers. Second, the shape of the flag covaried with those aspects of body shape that should reflect adaptation to different feeding regimes. Third, and most importantly, the shape of the flag covaried across populations with those environmental characteristics that should most closely reflect differences in local prey abundance. Overall, our results are consistent with a scenario where the evolution of this male sexual signal tracks food‐related shifts in female sensory biases across populations, thus providing at least provisional support for a role for sensory drive in population differentiation.     

Balanced polymorphisms and their divergence in a Heliconius butterfly

The evolution of mimicry in similarly defended prey is well described by the Müllerian mimicry theory, which predicts the convergence of warning patterns in order to gain the most protection from predators. However, despite this prediction, we can find great diversity of color patterns among Müllerian mimics such as Heliconius butterflies in the neotropics. Furthermore, some species have evolved the ability to maintain multiple distinct warning patterns in single populations, a phenomenon known as polymorphic mimicry. The adaptive benefit of these polymorphisms is questionable since variation from the most common warning patterns is expected to be disadvantageous as novel signals are punished by predators naive to them. In this study, we use artificial butterfly models throughout Central and South America to characterize the selective pressures maintaining polymorphic mimicry in Heliconius doris. Our results highlight the complexity of positive frequency‐dependent selection, the principal selective pressure driving convergence among Müllerian mimics, and its impacts on interspecific variation of mimetic warning coloration. We further show how this selection regime can both limit and facilitate the diversification of mimetic traits.     

Feature saltation and the evolution of mimicry

In Batesian mimicry, a harmless prey species imitates the warning coloration of an unpalatable model species. A traditional suggestion is that mimicry evolves in a two-step process, in which a large mutation first achieves approximate similarity to the model, after which smaller changes improve the likeness. However, it is not known which aspects of predator psychology cause the initial mutant to be perceived by predators as being similar to the model, leaving open the question of how the crucial first step of mimicry evolution occurs. Using theoretical evolutionary simulations and reconstruction of examples of mimicry evolution, we show that the evolution of Batesian mimicry can be initiated by a mutation that causes prey to acquire a trait that is used by predators as a feature to categorize potential prey as unsuitable. The theory that species gain entry to mimicry through feature saltation allows us to formulate scenarios of the sequence of events during mimicry evolution and to reconstruct an initial mimetic appearance for important examples of Batesian mimicry. Because feature-based categorization by predators entails a qualitative distinction between nonmimics and passable mimics, the theory can explain the occurrence of imperfect mimicry.     

Independent axes of genetic variation and parallel evolutionary divergence of opercle bone shape in threespine stickleback

Evolution of similar phenotypes in independent populations is often taken as evidence of adaptation to the same fitness optimum. However, the genetic architecture of traits might cause evolution to proceed more often toward particular phenotypes, and less often toward others, independently of the adaptive value of the traits. Freshwater populations of Alaskan threespine stickleback have repeatedly evolved the same distinctive opercle shape after divergence from an oceanic ancestor. Here we demonstrate that this pattern of parallel evolution is widespread, distinguishing oceanic and freshwater populations across the Pacific Coast of North America and Iceland. We test whether this parallel evolution reflects genetic bias by estimating the additive genetic variance-covariance matrix (G) of opercle shape in an Alaskan oceanic (putative ancestral) population. We find significant additive genetic variance for opercle shape and that G has the potential to be biasing, because of the existence of regions of phenotypic space with low additive genetic variation. However, evolution did not occur along major eigenvectors of G, rather it occurred repeatedly in the same directions of high evolvability. We conclude that the parallel opercle evolution is most likely due to selection during adaptation to freshwater habitats, rather than due to biasing effects of opercle genetic architecture.     

Antagonistic evolution in an aposematic predator–prey signaling system

Warning signals within species, such as the bright colors of chemically defended animals, are usually considered mutualistic, monomorphic traits. Such a view is however increasingly at odds with the growing empirical literature, showing nontrivial levels of signal variation within prey populations. Key to understanding this variation, we argue, could be a recognition that toxicity levels frequently vary within populations because of environmental heterogeneity. Inequalities in defense may undermine mutualistic monomorphic signaling, causing evolutionary antagonism between loci that determine appearance of less well‐defended and better defended prey forms within species. In this article, we apply a stochastic model of evolved phenotypic plasticity to the evolution of prey signals. We show that when toxicity levels vary, then antagonistic interactions can lead to evolutionary conflict between alleles at different signaling loci, causing signal evolution, “red queen‐like” evolutionary chase, and one or more forms of signaling equilibria. A key prediction is that variation in the way that predators use information about toxicity levels in their attack behaviors profoundly affects the evolutionary characteristics of the prey signaling systems. Environmental variation is known to cause variation in many qualities that organisms signal; our approach may therefore have application to other signaling systems.     

Non‐consumptive effects of predation: does perceived risk strengthen the genetic integration of behaviour and morphology in stickleback?

Predators can shape genetic correlations in prey by altering prey perception of risk. We manipulated perceived risk to test whether such non‐consumptive effects tightened behavioural trait correlations in wild‐caught stickleback from high‐ compared to low‐risk environments due to genetic variation in plasticity. We expected tighter genetic correlations within perceived risk treatments than across them, and tighter genetic correlations in high‐risk than in low‐risk treatments. We identified genetic variation in plasticity, with genetic correlations between boldness, sociality, and antipredator morphology, as expected, being tighter within treatments than across them, for both of two populations. By contrast, genetic correlations did not tighten with exposure to risk. Tighter phenotypic correlations in wild stickleback may thus arise because predators induce correlational selection on environmental components of these traits, or because predators tighten residual correlations by causing environmental heterogeneity that is controlled in the laboratory. Our study places phenotypic integration firmly into an ecological context.     

Prey community structure affects how predators select for Mullerian mimicry

Müllerian mimicry describes the close resemblance between aposematic prey species; it is thought to be beneficial because sharing a warning signal decreases the mortality caused by sampling by inexperienced predators learning to avoid the signal. It has been hypothesized that selection for mimicry is strongest in multi-species prey communities where predators are more prone to misidentify the prey than in simple communities. In this study, wild great tits (Parus major) foraged from either simple (few prey appearances) or complex (several prey appearances) artificial prey communities where a specific model prey was always present. Owing to slower learning, the model did suffer higher mortality in complex communities when the birds were inexperienced. However, in a subsequent generalization test to potential mimics of the model prey (a continuum of signal accuracy), only birds that had foraged from simple communities selected against inaccurate mimics. Therefore, accurate mimicry is more likely to evolve in simple communities even though predator avoidance learning is slower in complex communities. For mimicry to evolve, prey species must have a common predator; the effective community consists of the predator's diet. In diverse environments, the limited diets of specialist predators could create 'simple community pockets' where accurate mimicry is selected for.     

Experimental evolution of slowed cognitive aging in Drosophila melanogaster

Reproductive output and cognitive performance decline in parallel during aging, but it is unknown whether this reflects a shared genetic architecture or merely the declining force of natural selection acting independently on both traits. We used experimental evolution in Drosophila melanogaster to test for the presence of genetic variation for slowed cognitive aging, and assess its independence from that responsible for other traits’ decline with age. Replicate experimental populations experienced either joint selection on learning and reproduction at old age (Old + Learning), selection on late‐life reproduction alone (Old), or a standard two‐week culture regime (Young). Within 20 generations, the Old + Learning populations evolved a slower decline in learning with age than both the Old and Young populations, revealing genetic variation for cognitive aging. We found little evidence for a genetic correlation between cognitive and demographic aging: although the Old + Learning populations tended to show higher late‐life fecundity than Old populations, they did not live longer. Likewise, selection for late reproduction alone did not result in improved late‐life learning. Our results demonstrate that Drosophila harbor genetic variation for cognitive aging that is largely independent from genetic variation for demographic aging and suggest that these two aspects of aging may not necessarily follow the same trajectories.     

The dimensionality of genetic variation for wing shape in Drosophila melanogaster

Absolute constraints are limitations on genetic variation that preclude evolutionary change in some aspect of the phenotype. Absolute constraints may reflect complete absence of variation, lack of genetic variation that extends the range of phenotypes beyond some limit, or lack of additive genetic variation. This last type of absolute constraint is bidirectional, because the mean cannot evolve to be larger or smaller. Most traits do possess genetic variation, so bidirectional absolute constraints are most likely to be detected in a multivariate context, where they would reflect combinations of traits, or dimensions in phenotype space that cannot evolve. A bidirectional absolute constraint will cause the additive genetic covariance matrix (G) to have a rank less than the number of traits studied. In this study, we estimate the rank of the G-matrix for 20 aspects of wing shape in Drosophila melanogaster. Our best estimates of matrix rank are 20 in both sexes. Lower 95% confidence intervals of rank are 17 for females and 18 for males. We therefore find little evidence of bidirectional absolute constraints. We discuss the importance of this result for resolving the relative roles of selection and drift processes versus constraints in the evolution of wing shape in Drosophila.     

The evolution of warning signals as reliable indicators of prey defense

It is widely argued that defended prey have tended to evolve conspicuous traits because predators more readily learn to avoid defended prey when they are conspicuous. However, a rival theory proposes that defended prey have evolved such characters because it allows them to be distinguished from undefended prey. Here we investigated how the attributes of defended (unprofitable) and undefended (profitable) computer-generated prey species tended to evolve when they were subject to selection by foraging humans. When cryptic forms of defended and undefended species were similar in appearance but their conspicuous forms were not, defended prey became conspicuous while undefended prey remained cryptic. Indeed, in all of our experiments, defended prey invariably evolved any trait that enabled them to be distinguished from undefended prey, even if such traits were cryptic. When conspicuous mutants of defended prey were extremely rare, they frequently overcame their initial disadvantage by chance. When Batesian mimicry of defended species was possible, defended prey evolved unique traits or characteristics that would make undefended prey vulnerable. Overall, our work supports the contention that warning signals are selected for their reliability as indicators of defense rather than to capitalize on any inherent educational biases of predators.     

PREY ADAPTATION AS A CAUSE OF PREDATOR-PREY CYCLES

We analyze simple models of predator-prey systems in which there is adaptive change in a trait of the prey that determines the rate at which it is captured by searching predators. Two models of adaptive change are explored: (1) change within a single reproducing prey population that has genetic variation for vulnerability to capture by the predator; and (2) direct competition between two independently reproducing prey populations that differ in their vulnerability. When an individual predator's consumption increases at a decreasing rate with prey availability, prey adaptation via either of these mechanisms may produce sustained cycles in both species' population densities and in the prey's mean trait value. Sufficiently rapid adaptive change (e.g., behavioral adaptation or evolution of traits with a large additive genetic variance), or sufficiently low predator birth and death rates will produce sustained cycles or chaos, even when the predator-prey dynamics with fixed prey capture rates would have been stable. Adaptive dynamics can also stabilize a system that would exhibit limit cycles if traits were fixed at their equilibrium values. When evolution fails to stabilize inherently unstable population interactions, selection decreases the prey's escape ability, which further destabilizes population dynamics. When the predator has a linear functional response, evolution of prey vulnerability always promotes stability. The relevance of these results to observed predator-prey cycles is discussed.     

Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.     

Tasting the difference: do multiple defence chemicals interact in Müllerian mimicry?

Müllerian mimicry, where two unpalatable species share a warning pattern, is classically believed to be a form of mutualism, where the species involved share the cost of predator education. The evolutionary dynamics of Müllerian mimicry have recently become a controversial subject, after mathematical models have shown that if minor alterations are made to assumptions about the way in which predators learn and forget about unpalatable prey, this textbook case of mutualism may not be mutualistic at all. An underlying assumption of these models is that Müllerian mimics possess the same defence chemical. However, some Müllerian mimics are known to possess different defence chemicals. Using domestic chicks as predators and coloured crumbs flavoured with either the same or different unpalatable chemicals as prey, we provide evidence that two defence chemicals can interact to enhance predator learning and memory. This indicates that Müllerian mimics that possess different defence chemicals are better protected than those that share a single defence chemical. These data provide insight into how multiple defence chemicals are perceived by birds,and how they influence the way birds learn and remember warningly coloured prey. They highlight the importance of considering how different toxins in mimicry rings can interact in the evolution and maintenance of Müllerian mimicry and could help to explain the remarkable variation in chemical defences found within and between species.     

Evolutionary rates for multivariate traits: the role of selection and genetic variation

A fundamental question in evolutionary biology is the relative importance of selection and genetic architecture in determining evolutionary rates. Adaptive evolution can be described by the multivariate breeders'' equation (), which predicts evolutionary change for a suite of phenotypic traits () as a product of directional selection acting on them (β) and the genetic variance–covariance matrix for those traits (G). Despite being empirically challenging to estimate, there are enough published estimates of G and β to allow for synthesis of general patterns across species. We use published estimates to test the hypotheses that there are systematic differences in the rate of evolution among trait types, and that these differences are, in part, due to genetic architecture. We find some evidence that sexually selected traits exhibit faster rates of evolution compared with life-history or morphological traits. This difference does not appear to be related to stronger selection on sexually selected traits. Using numerous proposed approaches to quantifying the shape, size and structure of G, we examine how these parameters relate to one another, and how they vary among taxonomic and trait groupings. Despite considerable variation, they do not explain the observed differences in evolutionary rates.