The genetic basis of an adaptive radiation: warning colour in two Heliconius species

Mimetic colour pattern races of Heliconius butterflies provide a striking example of adaptive radiation and numerous crossing experiments have investigated the genetics of these racial differences. However, colour pattern differentiation between closely related Heliconius species has not been previously studied. Here we present data from crosses between H. erato cyrbia and its sister species, H. himera. The genetic architecture underlying colour pattern divergence between these species is identical to that observed between races of H. erato. As in inter-racial crosses, colour pattern differences resulted from segregation at a few major loci. Evidence from 1321 offspring in 4 F₁, 17 backcross, 7 F₂ and 21 further crosses showed that two major loci controlled most of the colour pattern differences between H. erato and H. himera. There were strong interactions between these loci in their patterns of expression and evidence for other loci with relatively minor phenotypic effects. More importantly, based on patterns of expression within broods and linkage with Aconitase, we conclude that these major loci were homologous with those known to be responsible for colour pattern differences within H. erato. Our crosses also permit a re-evaluation of the relationships between colour pattern races of H. erato. This suggests that H. e. hydara, which occurs across a major mtDNA break, is the ancestral phenotype from which other races have evolved. Based on this assumption, we find no evidence to support the recent suggestion that apparently homologous colour pattern alleles have arisen multiple times.     

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.     

Automimicry and the evolution of discrete prey defences

We consider the neglected question of how secondary defences of prey animals evolve if they are discontinuous in nature, being either present or absent, or expressible over a limited number of levels. We present a novel computer model that evaluates the conditions in which defended mutant prey may (1) fail to rise above nontrivial levels within a population, (2) reach values close to fixation, or (3) find some evolutionarily stable strategy (ESS) frequency between these two situations. Undefended prey that coexist with defended conspecifics are known as automimics. One finding is that automimicry can be an ESS over a range of conditions, but especially when prey are relatively cryptic and secondary defences are very effective at deterring predation. Evolutionarily stable automimicry emerges from the interplay between the direct benefits of costly defences in surviving individual attacks by predators and frequency-dependent benefits conferred on all prey, from a reduction in the rate of attack on all identical-looking prey. When, in contrast, secondary defences have continuous variation, the result is effectively a monomorphic state of defence across the population. Thus the degree and kind of variation that a defence takes has a profound effect on its initial evolution. We discuss the interesting possibility that mixed ESSs may help explain some examples of variation in prey secondary defences.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 393–402.     

The locomotory function of the fins in the squid Loligo pealei

Kinematic data of high spatial and temporal resolution, acquired from image sequences of adult long-finned squid, Loligo pealei, during steady swimming in a flume, were used to examine the role of fins and the coordination between fin and jet propulsion in squid locomotion. Fin shape and body outlines were digitized and used to calculate fin wave speed, amplitude, frequency, angle of attack, body deformation, speed, and acceleration. L. pealei were observed to have two fin gait patterns with a transition at 1.4-1.8 mantle lengths per second (L_m s^-1) marked by alternation between the two patterns. Fin motion in L. pealei exhibited characteristics of both traveling waves and flapping wings. At low speeds, fin motion was more wave-like; at high speeds, fin motion was more flap-like and was marked by regular periods during which the fins were wrapped tightly against the mantle. Fin cycle frequencies were dependent on swimming speed and gait, and obvious coordination between the fins and jet were observed. Fin wave speed, angle of attack, and body acceleration confirmed the role of fins in thrust production and revealed a role of fins at all swimming speeds by a transition from drag-based to lift-based thrust when fin wave speed dropped below swimming speed. Estimates of peak fin thrust were as high as 0.44-0.96 times peak jet thrust in steady swimming over the range of swimming speeds observed. Fin downstrokes generally contributed more to thrust than did upstrokes, especially at high speeds.     

The locomotory function of the fins in the squid Loligo pealei

Kinematic data of high spatial and temporal resolution, acquired from image sequences of adult long-finned squid, Loligo pealei, during steady swimming in a flume, were used to examine the role of fins and the coordination between fin and jet propulsion in squid locomotion. Fin shape and body outlines were digitized and used to calculate fin wave speed, amplitude, frequency, angle of attack, body deformation, speed, and acceleration. L. pealei were observed to have two fin gait patterns with a transition at 1.4-1.8 mantle lengths per second (Lm s-1) marked by alternation between the two patterns. Fin motion in L. pealei exhibited characteristics of both traveling waves and flapping wings. At low speeds, fin motion was more wave-like; at high speeds, fin motion was more flap-like and was marked by regular periods during which the fins were wrapped tightly against the mantle. Fin cycle frequencies were dependent on swimming speed and gait, and obvious coordination between the fins and jet were observed. Fin wave speed, angle of attack, and body acceleration confirmed the role of fins in thrust production and revealed a role of fins at all swimming speeds by a transition from drag-based to lift-based thrust when fin wave speed dropped below swimming speed. Estimates of peak fin thrust were as high as 0.44-0.96 times peak jet thrust in steady swimming over the range of swimming speeds observed. Fin downstrokes generally contributed more to thrust than did upstrokes, especially at high speeds.     

The effect of metapopulation dynamics on the survival and spread of a novel, conspicuous prey

Animals that deploy chemical defences against predators often signal their unprofitability using bright colouration. This pairing of toxicity and conspicuous patterning is known as aposematism.Explaining the evolution and spread of aposematic traits in previously cryptic species has been the focus of much empirical and theoretical work over the last two decades. Existing research concerning the initial evolution of aposematism does not however properly consider that many aposematic species (such as members of the hymenoptera, the lepidoptera, and amphibia) are highly mobile. We argue in this paper that the evolution of aposematic displays is therefore often best understood within a metapopulation framework; hence in this paper we present the first explicit metapopulation model of the evolution of aposematism. Our most general finding is that migration tends to reduce the probability that an aposematic prey can increase from rarity and spread across a large population. Hence, the best case scenarios for the spread of aposematism required fixation of the aposematic form in one or more isolated sub-habitats prior to some event which subsequently enabled migration. We observed that changes in frequency of new aposematic forms within source habitats are likely to be nonmonotonic. First, aposematic prey tend to decline in frequency as they migrate outwards from the source habitat to neighbouring sink habitats, but subsequently they increase in relative abundance in the source, as the descendents of earlier migrants migrate back from newly converted sub-populations. This pattern of initial loss and subsequent gain between new source and neighbouring sink habitats is then repeated as the aposematic form spreads via a moving cline.     

The association between amount of red muscle and mobility in fishes: A statistical evaluation

Synopsis It is commonly accepted that more active fishes have a greater proportion of red muscle in their trunk musculature than do less active fishes. Further, the proportion of red muscle has been used to classify fish species into functional groups reflecting different activity patterns. Nevertheless, existing measures of both red muscle and mobility have several limitations, and the relationship between these parameters has never been evaluated quantitatively. Using data from the literature, we demonstrate a positive, statistical association between the proportion of red muscle in the caudal peduncle of marine fishes and a qualitative measure of mobility (categorization as sedentary vs. mobile based on natural-history accounts). Analyses of the frequency distribution of the proportion of red muscle also provide evidence for two subdistributions. However, this bimodality does not correspond with sedentary vs. mobile or sit-and-wait vs. active search dichotomies.     

Effects of novelty and gregariousness in survival of aposematic prey

We examined the reactions of captive wild great tits to novelunpalatable prey with (1) a traditional aposematic signal (blackand yellow) (2) a novel signal (light pink), and (3) a controlsignal (brown). Prey were offered either singly or in groupsto see whether novel signals with fewer possibilities for synergisticbenefits are more dependent on grouping than are the traditionalsignals. Indeed, responses of birds toward unpalatable preydepended significantly on spatial distribution of prey (groupingversus solitary) and the type of the signal. Birds avoided morethe traditional black and yellow signals than novel pink signalsin both experimental set ups, but both of these prey items survivedbetter in aggregation than solitarily. The success of traditionalsignals may demonstrate the importance of synergistic selectionacross species in the evolution of warning coloration (i.e.,Müllerian mimicry). Unpalatable prey individuals benefitstrongly from using similar color patterns. Our results suggestthat aggregation may be important for the evolution of novelsignals in particular, even if a synergistic selection componentis also present     

Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies

Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases, signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here, we address this question in the aposematic passion‐vine butterfly Heliconius erato by using color‐ and pattern‐manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.     

Community structure and the evolution of aposematic coloration

Studies on the evolution of aposematic coloration (prey coloration advertising for unpalatability) have mainly focused on predator psychology in simplified single-prey species systems. We chose, instead, to model population dynamics on the community level. We studied the invasion by an aposematic phenotype in the presence and absence of another prey species. The single-prey and two-prey models differed in two major ways. First, with two prey species the invasion was possible only with a weak aposematic signal, whereas with a single prey species there was no such an upper limit for signal strength. Second, with a single prey species, increase of the aposematic phenotype always resulted in rapid extinction of the predator. Resource value and growth rate of the alternative prey species affected the invasion. These results suggest that community structure is an important determinant of the conditions for invasion of aposematism, and may have contributed to its initial evolution.     

The calcaneus of Australopithecus afarensis and its implications for the evolution of bipedality

Calcanei from African apes, modern humans, and Australopithecus afarensis are compared to investigate the anatomical and mechanical changes that occurred in this bone as a result of the transition to terrestrial bipedality. Features analyzed include the cross-sectional area and volume of the calcaneal tuber, the geometry and orientation of the articular surfaces, and the surface topography of the calcaneal corpus. Calcaneal morphology is unequivocal in its partitioning of quadrupedal pongids and bipedal hominids.     

The ischium and hip extensor mechanism in human evolution

Although it is commonly stated that the ischia of the late Pliocene–early Pleistocene hominid fossils are long and ape-like, new interpretations show this view to be fallacious. An important new theory proposed by Robinson concludes that the gracile form of early hominid was an efficient biped, but the robust form was a less efficient biped and was adapted for tree climbing. Interpretation of the ischium is crucial to this idea. The present study shows that (1) the gracile and robust australopithecine ischia had similar relative lengths and (2) that the hamstring mechanism was probably very similar in the two forms of South African early hominid.     

Optimal running speed and the evolution of hominin hunting strategies

Recent discussion of the selective pressures leading to the evolution of modern human postcranial morphology, seen as early as Homo erectus, has focused on the relative importance of walking versus running. Specifically, these conversations have centered on which gait may have been used by early Homo to acquire prey. An element of the debate is the widespread belief that quadrupeds are constrained to run at optimally efficient speeds within each gait, whereas humans are equally efficient at all running speeds. The belief in the lack of optimal running speeds in humans is based, however, on a number of early studies with experimental designs inadequate for the purpose of evaluating optimality. Here we measured the energetic cost of human running (n = 9) at six different speeds for five minutes at each speed, with careful replicates and controls. We then compared the fit of linear versus curvilinear models to the data within each subject. We found that individual humans do, in fact, have speeds at which running is significantly less costly than at other speeds (i.e., an optimal running speed). In addition, we demonstrate that the use of persistence hunting methods to gain access to prey at any running speed, even the optimum, would be extremely costly energetically, more so than a persistence hunt at optimal walking speed. We argue that neither extinct nor extant hominin populations are as flexible in the chosen speeds of persistence hunting pursuits as other researchers have suggested. Variations in the efficiency of human locomotion appear to be similar to those of terrestrial quadrupeds.     

Role of the MT-MTOC complex in determination of the cellular locomotory unit inDictyostelium

Summary The microtubule inhibitors, ethyl-N-phenylcarbamate (EPC) and thiabendazole (TB), which disrupt cytoplasmic microtubules and induce giant cells inDictyostelium (Kitanishi et al. 1984), were found to induce the occurrence of multiple microtubule organizing centers (MTOCs) in these giant cells. Probing was done by indirect immunofluorescence using monoclonal anti--tubulin. The nuclear DNA content of the giant cells increased in parallel with an increase in the number of MTOCs, as shown by microspectrophotometory of cells stained with the fluorescent DNA stain DAPI (4,6-diamidino-2-phenylindole).Shortly after the inhibitors were removed, the MTOCs of the giant cell formed multiple mitotic spindles or synchronously reconstituted numerous cytoplasmic MT-networks. These events apparently reflected the cell-cycle dependent activities of the MTOCs at the time the inhibitors were removed. When multiple spindles were formed, numerous cytoplasmic MT-networks became organized subsequent to the breakdown of the spindles. In either case, reconstitution of the cytoplasmic MT-networks was followed by apparently normal cytokinesis resulting in the production of many daughter cells each containing a single MT-MTOC complex. The evidence suggested the possible mechanism of the induction of multiple MTOCs, and implied that the MT-MTOC complex is significant in the cytokinesis ofDictyostelium by determining the cell locomotory unit.     

Postcranial adaptation and evolution in lorisidae

With the exception of leaping, lorises and galagos move in many similar ways although frequencies and styles differ. This peculiar locomotor distinction in two closely related subfamilies has profoundly altered their respective postcranial anatomies from their common ancestor. A comparison of postcranial adaptation in extant forms shows that lorises and galagos differ somewhat in forelimb mobility, but are more fundamentally disparate in hindlimb adaptation. Inferences concerning locomotor adaptation in the lorisid fossil record indicate a more generalized locomotor pattern which is more like that of extant cheirogaleids than either living galagos or lorises. Thus, vertical clinging and leaping in galagines and the slow-climbing and suspensory movements of lorisines appear to be evolutionarily recent innovations from a more generalized locomotor past.     

The energetic costs of load-carrying and the evolution of bipedalism

The evolution of habitual bipedalism is still a fundamental yet unsolved question for paleoanthropologists, and carrying is popular as an explanation for both the early adoption of upright walking and as a positive selection pressure once a terrestrial lifestyle had been adopted. However, to support or reject any hypothesis that suggests carrying efficiency was an important selective pressure, we need quantitative data on the costs of different forms of carrying behavior, especially infant-carrying since reduction in the grasping capabilities of the foot would have prevented infants from clinging on for long durations. In this study, we tested the hypothesis that the mode of load carriage influences the energetic cost of locomotion. Oxygen consumption was measured in seven female participants walking at a constant speed while carrying four different 10-kg loads (a weighted vest, 5-kg dumbbells carried in each hand, a mannequin infant carried on one hip, and a 10-kg dumbbell carried in a single hand). Oxygen consumption was also measured during unloaded standing and unloaded walking. The results show that the weighted vest requires the least amount of energy of the four types of carrying and that, for this condition, humans are as efficient as mammals in general. The balanced load was carried with approximately the predicted energy cost. However, the asymmetrical conditions were considerably less efficient, indicating that, unless infant-carrying was the adaptive response to a strong environmental selection pressure, this behavior is unlikely to have been the precursor to the evolution of bipedalism.     

Predation and the evolution of prey behavior: an experiment with tree hole mosquitoes

We tested for facultative changes in behavior of an aquaticinsect in response to cues from predation and for evolutionof prey behavior in response to experimental predation regimes.Larvae of the tree hole mosquito Aedes triseriatus reducedfiltering, browsing, and time below the surface in responseto water that had held a feeding larva of the predator Toxorhynchitesrutilus. We subjected experimental A. triseriatus populationsto culling of 50% of the larval population, either by T. rutiluspredation or by random removal. After two generations of laboratoryculling, behavior of the two treatment groups diverged. Aedestriseriatus in control-culled lines retained their facultativeshift from filtering to resting, but tended to lose the response of reduced browsing below the surface in water that had helda feeding predator. Predator-culled lines lost their facultativeresponse of reduced filtering in water that had held a feedingpredator and evolved toward more time resting and less timefiltering in both water that had held a feeding predator andwater that had held only A. triseriatus. Predator-culled linesretained their facultative response of reduced browsing belowthe surface in water that had held a feeding predator. Twofield populations and their reciprocal hybrids responded similarlyto cues from predation and did not differ in their evolutionaryresponse to experimental culling. We conclude that consistentpresence or absence of predation can select rapidly for divergencein prey behavior, including facultative behavioral responsesto predators.     

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.