The (Under)Use of Eye-Tracking in Evolutionary Ecology.

To survive and pass on their genes, animals must perform many tasks that affect their fitness, such as mate-choice, foraging, and predator avoidance. The ability to make rapid decisions is dependent on the information that needs to be sampled from the environment and how it is processed. We highlight the need to consider visual attention within sensory ecology and advocate the use of eye-tracking methods to better understand how animals prioritise the sampling of information from their environments prior to making a goal-directed decision. We consider ways in which eye-tracking can be used to determine how animals work within attentional constraints and how environmental pressures may exploit these limitations.

Widespread Wolbachia infection in an insular radiation of damselflies (Odonata, Coenagrionidae).

Wolbachia is one of the most common endosymbionts found infecting arthropods. Theory predicts symbionts like Wolbachia will be more common in species radiations, as host shift events occur with greatest frequency between closely related species. Further, the presence of Wolbachia itself may engender reproductive isolation, and promote speciation of their hosts. Here we screened 178 individuals belonging to 30 species of the damselfly genera Nesobasis and Melanesobasis - species radiations endemic to the Fiji archipelago in the South Pacific - for Wolbachia, using multilocus sequence typing to characterize bacterial strains. Incidence of Wolbachia was 71% in Nesobasis and 40% in Melanesobasis, and prevalence was also high, with an average of 88% in the Nesobasis species screened. We identified a total of 25 Wolbachia strains, belonging to supergroups A, B and F, with some epidemic strains present in multiple species. The occurrence of Wolbachia in both males and females, and the similar global prevalence found in both sexes rules out any strong effect of Wolbachia on the primary sex-ratio, but are compatible with the phenotype of cytoplasmic incompatibility. Nesobasis has higher species richness than most endemic island damselfly genera, and we discuss the potential for endosymbiont-mediated speciation within this group.

The evolution of respect for property.

Although possession is 'nine-tenths of the law', respect for ownership is widespread in the animal kingdom even without third-party enforcement. Thus, the first individuals to find objects are frequently left unchallenged by potential competitors and tend to win contests when disputes arise. Game theory has shown that respect for ownership ('Bourgeois' behaviour) can arise as an arbitrary convention to avoid costly disputes. However, the same theory predicts that a paradoxical respect for lack of ownership ('anti-Bourgeois' behaviour) can evolve under the same conditions and in some cases is the only stable outcome. Despite these predictions, anti-Bourgeois behaviour is rare in nature, whereas respect for ownership is frequently not absolute. Here, we review extensions of the classic models involving repeated interactions, confusion over roles, strategic coordination of behaviour ('secret handshakes'), owner-intruder asymmetries and continuous control of fighting investment. Confusion over roles and owner-intruder asymmetries in fighting ability may explain why respect for ownership is often partial. Moreover, although most model extensions facilitate the evolution of Bourgeois-like behaviour, secret handshakes and continuous control of fighting investment render the alternative anti-Bourgeois convention unstable. We develop these insights to highlight several key areas for future investigation.

Species with a chemical defence, but not chemical offence, live longer.

Evolutionary hypotheses for ageing generally predict that delayed senescence should evolve in organisms that experience lower extrinsic mortality. Thus, one might expect species that are highly toxic or venomous (i.e. chemically protected) will have longer lifespans than related species that are not likewise protected. This remarkable relationship has been suggested to occur in amphibians and snakes. First, we show that chemical protection is highly conserved in several lineages of amphibians and snakes. Therefore, accounting for phylogenetic autocorrelation is critical when conservatively testing evolutionary hypotheses because species may possess similar longevities and defensive attributes simply through shared ancestry. Herein, we compare maximum longevity of chemically protected and nonprotected species, controlling for potential nonindependence of traits among species using recently available phylogenies. Our analyses confirm that longevity is positively correlated with body size in both groups which is consistent with life-history theory. We also show that maximum lifespan was positively associated with chemical protection in amphibian species but not in snakes. Chemical protection is defensive in amphibians, but primarily offensive (involved in prey capture) in snakes. Thus, we find that although chemical defence in amphibians favours long life, there is no evidence that chemical offence in snakes does the same.

A comparative analysis of senescence in adult damselflies and dragonflies (Odonata).

Any population whose members are subject to extrinsic mortality should exhibit an increase in mortality with age. Nevertheless, the prevailing opinion is that populations of adult damselflies and dragonflies do not exhibit such senescence. Here, we challenge this contention by fitting a range of demographic models to the data on which these earlier conclusions were based. We show that a model with an exponential increase in age-related mortality (Gompertz) generally provides a more parsimonious fit than alternative models including age-independent mortality, indicating that many odonates do indeed senesce. Controlling for phylogeny, a comparison of the daily mortality of 35 odonate species indicates that although male and female mortalities are positively correlated, mortality tends to be higher in males of those species that exhibit territoriality. Hence, we show for the first time that territoriality may impose a survivorship cost on males, once the underlying phylogenetic relationships are accounted for.

Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera).

1. Age-dependent increases in mortality have been documented in a variety of species of insect under laboratory conditions. However, while strong statistical evidence has been presented for senescence in vertebrate populations in the wild, we know little about the rate and shape of senescence in wild populations of insects. 2. Odonates (damselflies and dragonflies) provide excellent candidate species for evaluating demographic senescence as they are large enough to be marked individually and they are easily re-sighted without recapture. The prevailing opinion - based entirely on qualitative examination of the declines in log numbers alive with time since marking - is that odonates exhibit age-independent daily survivorship. 3. Here, we examine mark-recapture data on the Azure Damselfly Coenagrion puella over two consecutive seasons. For the first time, we evaluate and compare the fit of quantitative models that not only account for weather-dependent daily variation in daily re-sighting rates, but also age-dependent variation in daily survivorship. 4. Models with age-dependent declines in daily survivorship provide a more parsimonious explanation for the data than similar models without these age-dependent effects. In general, models in which mortality increases in an exponential (Gompertz) fashion explain the mark-recapture sequences more efficiently than a range of alternative models, including those in which mortality increases as a power function (Weibull) or reaches a plateau (logistic). These results are indicative of a general senescent decline in physiological functioning, which is particularly marked after 15 days as a mature adult. 5. Weather (temperature, sun and precipitation) and initial mite load influenced the probability of daily re-sighting. Weather and mite load also influenced daily survivorship, but their effects differed between seasons. 6. Overall, fitting models with age as an explicit covariate demonstrates that odonates do indeed senesce. This contradicts previously held assumptions that Odonata do not exhibit age-dependent survivorship in the wild.

The evolution of senescence through decelerating selection for system reliability.

Senescence is a universal phenomenon in organisms, characterized by increasing mortality and decreasing fecundity with advancing chronological age. Most proximate agents of senescence, such as reactive oxygen species and UV radiation, are thought to operate by causing a gradual build-up of bodily damage. Yet most current evolutionary theories of senescence emphasize the deleterious effects of functioning genes in late life, leaving a gap between proximate and ultimate explanations. Here, we present an evolutionary model of senescence based on reliability theory, in which beneficial genes or gene products gradually get damaged and thereby fail, rather than actively cause harm. Specifically, the model allows organisms to evolve multiple redundant copies of a gene product (or gene) that performs a vital function, assuming that organisms can avoid condition-dependent death so long as at least one copy remains undamaged. We show that organisms with low levels of extrinsic mortality, and high levels of genetic damage, tend to evolve high levels of redundancy, and that mutation-selection balance results in a stable population distribution of the number of redundant elements. In contrast to previous evolutionary models of senescence, the mortality curves that emerge from such populations match empirical senescence patterns in three key respects: they exhibit: (1) an initially low, but rapidly increasing mortality rate at young ages, (2) a plateau in mortality at advanced ages and (3) 'mortality compensation', whereby the height of the mortality plateau is independent of the environmental conditions under which different populations evolved.

Evasive mimicry: when (if ever) could mimicry based on difficulty of capture evolve?

We elucidate the conditions under which an easy-to-catch edible prey species may evolve to resemble another edible species that is much more difficult to capture ('evasive Batesian mimicry'), and the conditions under which two or more edible but hard-to-catch species evolve a common resemblance ('evasive Mullerian mimicry'). Using two complementary mathematical models, we argue that both phenomena are logically possible but that several factors will limit the prevalence of these forms of mimicry in nature. Evasive Batesian mimicry is most likely to arise when it is costly in time or energy for the predator species to pursue evasive prey, when mimics are encountered less frequently than evasive models and where there are abundant alternative prey. Evasive Mullerian mimicry, by contrast, is most likely to arise when evasive prey species differ in abundance, predators are slow to learn to avoid evasive prey and evading capture is costly to the prey. Unequivocal evidence for evasive Batesian or Mullerian mimicry has not yet been demonstrated in the field, and we argue that more empirical work is needed to test whether putative examples are indeed a result of selection to signal difficulty of capture.

The effects of the size and shape of landscape features on the formation of traveling waves in cyclic populations.

Recent field data indicate that in a number of cyclic populations, the cycles are organized spatially with the form of a periodic traveling wave. One way in which this type of wave is generated is when dispersing individuals encounter landscape features that impede movement in certain directions. In this article, we investigate the dependence of such periodic waves on ecological parameters and on the form of the landscape feature. Using a standard predator-prey model as a prototype for a cyclic population, we calculate the speed and amplitude of waves generated by a large landscape feature. This enables us to determine parameters for which the waves are stable; in other cases, they evolve into irregular oscillations. We then undertake for the first time a detailed study of the effects of the size and shape of a landscape feature on the waves that it generates. We show that size rather than shape is the key wave-forming property, with smaller obstacles generating waves with longer wavelength and waves from larger landscape features dominating those from smaller ones. Our results suggest that periodic traveling waves may be much more common than has previously been assumed in real ecological systems, and they enable quantitative predictions on the properties of these waves for particular cases.

Sex-specific foraging behaviour in a monomorphic seabird.

Sexual differences in the foraging behaviour of parents have been observed in a number of sexually sizedimorphic birds, particularly seabirds, and the usual inference has been that these sex-specific differences are mediated primarily by differences in body size. To test this explanation, we compared the foraging behaviour of parents in a monomorphic seabird species, the northern gannet Morus bassanus. Using specially designed instruments and radio telemetry we found that individuals of both sexes were consistent in the directions and durations of their foraging trips. However, there were significant differences in the foraging behaviour of males and females. Female gannets were not only more selective than males in the areas where they foraged, but they also made longer, deeper dives and spent more time on the sea surface than males. As the sexes are morphologically similar in this species, then these differences are unlikely to have been mediated by body size. Our work highlights the need to investigate sexual differences in the foraging behaviour of seabirds and other species more closely, in order to test alternative theories that do not rely on differences in body size.

Generation of periodic waves by landscape features in cyclic predator-prey systems.

The vast majority of models for spatial dynamics of natural populations assume a homogeneous physical environment. However, in practice, dispersing organisms may encounter landscape features that significantly inhibit their movement. We use mathematical modelling to investigate the effect of such landscape features on cyclic predator-prey populations. We show that when appropriate boundary conditions are applied at the edge of the obstacle, a pattern of periodic travelling waves develops, moving out and away from the obstacle. Depending on the assumptions of the model, these waves can take the form of roughly circular 'target patterns' or spirals. This is, to our knowledge, a new mechanism for periodic-wave generation in ecological systems and our results suggest that it may apply quite generally not only to cyclic predator-prey interactions, but also to populations that oscillate for other reasons. In particular, we suggest that it may provide an explanation for the observed pattern of travelling waves in the densities of field voles (Microtus agrestis) in Kielder Forest (Scotland-England border) and of red grouse (Lagopus lagopus scoticus) on Kerloch Moor (northeast Scotland), which in both cases move orthogonally to any large-scale obstacles to movement. Moreover, given that such obstacles to movement are the rule rather than the exception in real-world environments, our results suggest that complex spatio-temporal patterns such as periodic travelling waves are likely to be much more common in the natural world than has previously been assumed.

Evidence of intra-specific competition for food in a pelagic seabird.

The factors affecting the population dynamics of seabirds have long intrigued biologists. Current data suggest that density-dependent depletion of prey during the breeding season may regulate population size. However, much of the evidence for this has been circumstantial, and the underlying mechanisms are unclear. Here, we show that the per capita population growth rates of northern gannet Morus bassanus at colonies in Britain and Ireland have declined with increasing population size. Furthermore, direct observations reveal that the mean foraging trip duration of breeding gannets is positively correlated with colony size, both among colonies of different sizes in the same year, and within colonies as they change in size. To understand this phenomenon, we have developed a model which demonstrates that disturbance of fish alone can readily generate conditions under which gannets at larger colonies have to travel further to obtain food.

The evolution of quantitatively responsive cooperative trade.

The iterated Prisoner's Dilemma reflects the essence of repeated cooperative interactions with selfish incentives. However, the classical form of this game assumes that individuals either cooperate or defect, whereas in practice different degrees of cooperation are usually possible. To overcome this limitation, we present a model of alternating cooperative trade in which individuals controlled the costs they incurred in benefiting their partners. Since the range of possible strategies is enormous, competitively successful solutions were identified using a genetic algorithm, a powerful search technique in which good performers are iteratively selected and recombined from an initial "strategy soup". Beginning with a population of asocial individuals, altruistic behaviour readily emerged. Like the pre-defined strategy of "Raise-the-Stakes", the emerging strategies evolved protection from cheats by investing relatively little in strangers and subsequently responding quantitatively to a partner's altruism. Unlike "Raise-the-Stakes", they began trading relations at intermediate levels and, when the benefit-to-cost ratio of cooperation was relatively low, mean investment was considerably below the maximum level. Our approach is novel in allowing us to predict not just whether cooperation will occur, but how cooperative individuals will be, in relation to factors such as the number of rounds and the cost effectiveness of cooperative trade.

Genetic variation within a parthenogenetic lineage.

A clone of the grain aphid Sitobion avenae F. was maintained parthenogenetically over thirty-two generations (n = 344) in a constant environment: a new generation being set up by a female selected at random from the preceding generation. Genomic DNA from individual aphids was screened for genetic stability using RAPD-PCR with a previously tested ten-mer primer. A putative germ-line mutation was noted in generation 14 and somatic mutations were noted in generations 12, 25, 27 and 29. There were no differences in the RAPD-PCR profiles of winged and wingless morphs and samples tested for symbiotic DNA. No endoblotic fungal organism was associated with the clone. Southern blotting and hybridization studies indicated that band additions were of aphid origin. However, the RAPD-PCR profiles of the germ-line and somatic mutation samples were unique from other aphid clones cultured during the experimental period. This paper documents discernible genetic changes occurring within an animal clonal lineage over time and Impacts on the consequences this may have for clonal systems.

The evolution of generosity and choosiness in cooperative exchanges.

In this paper we present a resource-explicit Donor-Receiver model for reciprocally altruistic interactions that obeys the defining inequalities of the Prisoner's Dilemma. In our model, individuals vary in the quantity of resource they invest when cooperating (termed "generosity") and they have the freedom to opt out of interactions with potential partners on the basis of their past experiences with these players (termed "choosiness"). Dynamic optimal solutions were found using a genetic algorithm in which the decision rules (cooperate or defect), generosity when cooperating, and choosiness exhibited by individuals when deciding to opt out, were all coded on genes held on two separate chromosomes. Through this genetic algorithm, individuals that had alleles which resulted in greatest success at playing our modified Prisoner's Dilemma left more offspring. When the benefit of receiving a unit resource exceeded the cost of giving, then generous cooperative behaviour tended to emerge within the population, even when the alleles of all the individuals in the starting population were set to defect. When the probability of individuals re-encountering one another was increased, individuals not only cooperated more, but they developed greater generosity. However, as the ratio of the benefits received to costs expended increased above 1, individuals in this model remained highly cooperative but their median generosity decreased significantly. In contrast to earlier studies using genetic algorithms, the extra potential for cheating afforded by asymmetrical degrees of generosity meant that genuinely cooperative behaviour did not emerge in the equivalent round-robin tournament in which individuals were not able to exercise partner preference.

Development of cooperative relationships through increasing investment.

Reciprocal altruism can become established among selfish, unrelated individuals if they use responsive strategies such as 'tit-for-tat. This result raises the fundamental question: how altruistic should one be? The problem is difficult to solve using current 'prisoner's dilemma' based models because they allow only the discrete choice of cooperating or defecting. In reality, however, cooperation is rarely all-or-nothing. Furthermore, if cooperative investment is variable, a new and more subtle kind of cheating becomes possible: individuals may invest slightly less than their partner. A concern is that this 'short-changing' will erode cooperative ventures. Here we show that cooperation can thrive despite variable investment through the new strategy of 'raise-the-stakes'. This strategy offers a small amount on first meeting and then, if matched, raises its investment, something that no strategy in the discrete model can do. We show that such behaviour can readily invade a population of non-altruists and cannot be effectively exploited. The practice of 'testing the water' rather than making sudden cooperative 'leaps of faith' powerfully reinforces the stability and effectiveness of reciprocity.

Spatial and temporal genetic variation in British field populations of the grain aphid Sitobion avenae (F.) (Hemiptera: Aphididae) studied using RAPD-PCR.

The grain aphid Sitobion avenae (F.) was collected from winter wheat and adjacent cocksfoot grass at two locations in southern England and at four times in the year (April-July). Genetic variation between individual aphids was then investigated using random amplified polymorphic DNA polymerase chain reaction. Individuals caught in wheat and cocksfoot during April provided very different and highly diagnostic banding patterns that were independent of location. This host-based genetic differentiability was less evident as the season progressed, largely as a result of genetic drift and local movement between adjacent host species, which appeared to be predominantely in the direction from cocksfoot to wheat. The diversity of putative clones fell significantly, the mean number of individuals per clone rose and clones became more exclusively associated with certain sites which suggests that long-distance migration may have less of a homogenizing effect than hitherto thought for this species.

Geographic and microgeographic genetic differentiation in two aphid species over southern England using the multilocus (GATA)4 probe.

Samples of the grain aphid Sitobion avenae (F.) and the rose-grain aphid Metopolophium dirhodum (Walker) were collected in late March from wheat fields and adjacent road-side grasses at a number of locations in southern England. Unparasitized aphids were DNA fingerprinted using the multilocus (GATA)4 probe. Over all locations, the fingerprints of individual S. avenae caught in wheat had lower overall average distances of band migration (ADBM) and shared a higher proportion of bands, than fingerprints of individuals caught in adjacent road-side grasses. The ADBM of fingerprints of S. avenae collected on road-side grasses altered significantly with geographical location, while the ADBM of fingerprints of S. avenae caught on wheat did not. A comparison of the fingerprints of individual M. dirhodum caught in wheat and neighbouring road-side grasses did not reveal any genetic differentiation. Fingerprints of M. dirhodum that were caught in the same host type did however, show significant variation in ADBM between different locations. With both S. avenae and M. dirhodum, spatial autocorrelation revealed that locations that were close together were no more likely to have individuals with similar ADBM than locations that were far apart. Our results suggest that (i) particular clones of S. avenae prefer to colonize wheat, and/or that (ii) particular clones of S. avenae perform better on wheat than other clones. It is unclear why M. dirhodum did not show any genetic structuring according to host type, but this species appears to engage in sexual reproduction much more frequently than S. avenae in southern England.(ABSTRACT TRUNCATED AT 250 WORDS)

An investigation of the differential performance of clones of the aphid Sitobion avenae on two host species.

Individuals of the grain aphid Sitobion avenae were collected from wheat and cocksfoot stands around Hampshire, UK, during March and April 1994. Eight wheat and eight cocksfoot aphid clones were chosen on the basis of readily distinguishable RAPD-PCR fingerprint profiles. The performances (weight, fecundity and survival) of successive generations of each of these clones were then carefully monitored in the laboratory as new generations of aphids were transferred either to winter wheat or to cocksfoot in planned sequences. Even those clones that were originally caught on the same host showed significant variability in performance. Clones generally performed better on their host of origin than they did on the alternate host, and they performed less well on the alternate host compared to the clones that had originated there. A comparison of the performance of third generation aphids with first generation aphids showed that the experience of the mother in the second generation often influences the subsequent performance of their offspring. As the sequence of host transfers had more effect on the performance of wheat clones than cocksfoot clones, it is likely that wheat clones are more specialised, such that wheat is a satisfactory host for cocksfoot clones but not vice versa. The study provides evidence of genetic variation in performance on host and evidence for clonal adaptation to particular host species. This adaptation may well be a major cause of the observed consistent genetic differentiability of populations of S. avenae found on wheat and roadside grasses in early spring in southern England.

An analysis of secondary spread by putative clones of Sitobion avenae within a Hampshire wheat field using the multilocus (GATA)4 probe.

Grain aphids (Sitobion avenae (F.)) were collected from forty-four wheat ears in a Hampshire field at three times during the growing season. On each occasion, individual aphids were profiled using the multilocus (GATA)4 probe. During the full head emergence and full anthesis growth stages of wheat, each ear generally supported a genetically distinguishable aphid colony which consisted of genetically indistinguishable individuals (putative clones). This information strongly suggests that individual ears were colonized by single immigration events. By the late milky ripe stage, most ears supported two or more such clones. The total number of clones declined and the spatial separation of identical clones increased markedly over the duration of the study, which strongly suggests that secondary spread rather than increased immigration was responsible for the increased clonal diversity of ears. In addition, the profiles of individual S. avenae became more alike as the season progressed and samples became dominated by particular clones indicating either differential survival or reproduction among clones.