Animals, including dogs, dolphins, monkeys and man, follow gaze. What mediates this bias towards the eyes? One hypothesis is that primates possess a distinct neural module that is uniquely tuned for the eyes of others. An alternative explanation is that configural face processing drives fixations to the middle of peoples' faces, which is where the eyes happen to be located. We distinguish between these two accounts. Observers were presented with images of people, non-human creatures with eyes in the middle of their faces (`humanoids’) or creatures with eyes positioned elsewhere (`monsters’). There was a profound and significant bias towards looking early and often at the eyes of humans and humanoids and also, critically, at the eyes of monsters. These findings demonstrate that the eyes, and not the middle of the head, are being targeted by the oculomotor system.
gaze following; gaze selection; social attention; primates
Infection with parasites and pathogens is costly for hosts, causing loss of nutritional resources, reproductive potential, tissue integrity and even life. In response, animals have evolved behavioural and immunological strategies to avoid infection by pathogens and infestation by parasites. Scientists generally study these strategies in isolation from each other; however, since these defences entail costs, host individuals should benefit from balancing investment in these strategies, and understanding of infectious disease dynamics would benefit from studying the relationship between them. Here, we show that Carpodacus mexicanus (house finches) avoid sick individuals. Moreover, we show that individuals investing less in behavioural defences invest more in immune defences. Such variation has important implications for the dynamics of pathogen spread through populations, and ultimately the course of epidemics. A deeper understanding of individual- and population-level disease defence strategies will improve our ability to understand, model and predict the outcomes of pathogen spread in wildlife.
disease avoidance; ecoimmunology; behaviour; innate immune function; house finch
Vocal duetting occurs in many taxa, but its function remains much-debated. Like species in which only one sex sings, duetting birds can use their song repertoires to signal aggression by singing song types that match those of territorial intruders. However, when pairs do not share specific combinations of songs (duet codes), individuals must choose to signal aggression by matching the same-sex rival, or commitment by replying appropriately to their mate. Here, we examined the song types used by female happy wrens (Pheugopedius felix) forced to make this decision in a playback experiment. We temporarily removed the male from the territory and then played songs from two loudspeakers to simulate an intruding female and the removed mate's response, using song types that the pair possessed but did not naturally combine into duets. Females were aggressive towards the female playback speaker, approaching it and overlapping the female playback songs, but nevertheless replied appropriately to their mate's songs instead of type matching the intruding female. This study indicates that females use song overlapping to signal aggression but use their vocal repertoires to create pair-specific duet codes with their mates, suggesting that duetting functions primarily to demonstrate pair commitment.
duetting; song matching; happy wren; territory defence; cooperation
Male homosexual behaviour—although found in most extant clades across the Animal Kingdom—remains a conundrum, as same-sex mating should decrease male reproductive fitness. In most species, however, males that engage in same-sex sexual behaviour also mate with females, and in theory, same-sex mating could even increase male reproductive fitness if males improve their chances of future heterosexual mating. Females regularly use social information to choose a mate; e.g. male attractiveness increases after a male has interacted sexually with a female (mate choice copying). Here, we demonstrate that males of the tropical freshwater fish Poecilia mexicana increase their attractiveness to females not only by opposite-sex, but likewise, through same-sex interactions. Hence, direct benefits for males of exhibiting homosexual behaviour may help explain its occurrence and persistence in species in which females rely on mate choice copying as one component of mate quality assessment.
homosexuality; mate choice copying; non-independent mate choice; same-sex mating
In cooperative breeders, sexually mature subordinates can either queue for chances to inherit the breeding position in their natal group, or disperse to reproduce independently. The choice of one or the other option may be flexible, as when individuals respond to attractive dispersal options, or they may reflect fixed life-history trajectories. Here, we show in a permanently marked, natural population of the cooperatively breeding cichlid fish Neolamprologus pulcher that subordinate helpers reduce investment in territory defence shortly before dispersing. Such reduction of effort is not shown by subordinates who stay and inherit the breeding position. This difference suggests that subordinates ready to leave reduce their investment in the natal territory strategically in favour of future life-history perspectives. It seems to be part of a conditional choice of the dispersal tactic, as this reduction in effort appears only shortly before dispersal, whereas philopatric and dispersing helpers do not differ in defence effort earlier in life. Hence, cooperative territory defence is state-dependent and plastic rather than a consistent part of a fixed life-history trajectory.
cooperative breeding; dispersal; consistent behavioural variation; life history; helping; Neolamprologus pulcher
Stressful conditions experienced by individuals during their early development have long-term consequences on various life-history traits such as survival until first reproduction. Oxidative stress has been shown to affect various fitness-related traits and to influence key evolutionary trade-offs but whether an individual's ability to resist oxidative stress in early life affects its survival has rarely been tested. In the present study, we used four years of data obtained from a free-living great tit population (Parus major; n = 1658 offspring) to test whether pre-fledging resistance to oxidative stress, measured as erythrocyte resistance to oxidative stress and oxidative damage to lipids, predicted fledging success and local recruitment. Fledging success and local recruitment, both major correlates of survival, were primarily influenced by offspring body mass prior to fledging. We found that pre-fledging erythrocyte resistance to oxidative stress predicted fledging success, suggesting that individual resistance to oxidative stress is related to short-term survival. However, local recruitment was not influenced by pre-fledging erythrocyte resistance to oxidative stress or oxidative damage. Our results suggest that an individual ability to resist oxidative stress at the offspring stage predicts short-term survival but does not influence survival later in life.
oxidative stress; early-life conditions; local recruitment; fledging success; Parus major
Late Pliocene climate changes have long been implicated in environmental changes and mammalian evolution in Africa, but high-resolution examinations of the fossil and climatic records have been hampered by poor sampling. By using fossils from the well-dated Shungura Formation (lower Omo Valley, northern Turkana Basin, southern Ethiopia), we investigate palaeodietary changes in one bovid and in one suid lineage from 3 to 2 Ma using stable isotope analysis of tooth enamel. Results show unexpectedly large increases in C4 dietary intake around 2.8 Ma in both the bovid and suid, and possibly in a previously reported hippopotamid species. Enamel δ13C values after 2.8 Ma in the bovid (Tragelaphus nakuae) are higher than recorded for any living tragelaphin, and are not expected given its conservative dental morphology. A shift towards increased C4 feeding at 2.8 Ma in the suid (Kolpochoerus limnetes) appears similarly decoupled from a well-documented record of dental evolution indicating gradual and progressive dietary change. The fact that two, perhaps three, disparate Pliocene herbivore lineages exhibit similar, and contemporaneous changes in dietary behaviour suggests a common environmental driver. Local and regional pollen, palaeosol and faunal records indicate increased aridity but no corresponding large and rapid expansion of grasslands in the Turkana Basin at 2.8 Ma. Our results provide new evidence supporting ecological change in the eastern African record around 2.8 Ma, but raise questions about the resolution at which different ecological proxies may be comparable, the correlation of vegetation and faunal change, and the interpretation of low δ13C values in the African Pliocene.
stable isotope analysis; palaeoecology; diet; Africa; Pliocene
When two dissimilar colours are displayed to the two eyes at overlapping retinal locations, binocular rivalry typically results: a fluctuating struggle for perceptual dominance of each eye's stimulus. We found instead that isoluminant counter-rotating patterns consisting of coloured and achromatic portions can promote an illusory colour ‘misbinding’, where the colours from both eyes were perceived within a single rotating pattern. The achromatic portion of one rotating pattern thus appeared to take on the colour of the other, oppositely rotating pattern. The results suggest that the neural mechanisms of colour binding can operate even while representations of the same patterns' motions are undergoing rivalry, and support the idea that rivalry can occur in isolation within the motion system.
binocular rivalry; primate vision; colour; motion; binding; parallel pathways
The Tasmanian devil (Sarcophilus harrisii) is at risk of extinction owing to the emergence of a contagious cancer known as devil facial tumour disease (DFTD). The emergence and spread of DFTD has been linked to low genetic diversity in the major histocompatibility complex (MHC). We examined MHC diversity in historical and ancient devils to determine whether loss of diversity is recent or predates European settlement in Australia. Our results reveal no additional diversity in historical Tasmanian samples. Mainland devils had common modern variants plus six new variants that are highly similar to existing alleles. We conclude that low MHC diversity has been a feature of devil populations since at least the Mid-Holocene and could explain their tumultuous history of population crashes.
Sarcophilus harrisii; major histocompatibility complex
We routinely form impressions of people from their faces, and these impressions sometimes contain a kernel of truth. Impressions of trustworthiness are central to interpersonal relationships, but their accuracy remains contentious. Here, we investigated whether sexual trustworthiness (faithfulness) can be accurately judged from opposite-sex strangers' faces. Women's ratings of men's unfaithfulness showed small–moderate correlations with men's past unfaithfulness (cheating, poaching). Women used masculinity as a valid cue to unfaithfulness. Men's unfaithfulness ratings showed small, non-significant correlations with unfaithfulness, although formal tests for sex differences yielded equivocal results. Women were less likely than men to erroneously classify unfaithful individuals as faithful. We conclude that impressions of sexual faithfulness from faces have a kernel of truth, at least for women, and that they may help people assess the quality of potential mates about whom they have minimal behavioural information.
face perception; infidelity; trustworthiness; evolutionary psychology
Animal ecology is shaped by energy costs, yet it is difficult to measure fine-scale energy expenditure in the wild. Because metabolism is often closely correlated with mechanical work, accelerometers have the potential to provide detailed information on energy expenditure of wild animals over fine temporal scales. Nonetheless, accelerometry needs to be validated on wild animals, especially across different locomotory modes. We merged data collected on 20 thick-billed murres (Uria lomvia) from miniature accelerometers with measurements of daily energy expenditure over 24 h using doubly labelled water. Across three different locomotory modes (swimming, flying and movement on land), dynamic body acceleration was a good predictor of daily energy expenditure as measured independently by doubly labelled water (R2 = 0.73). The most parsimonious model suggested that different equations were needed to predict energy expenditure from accelerometry for flying than for surface swimming or activity on land (R2 = 0.81). Our results demonstrate that accelerometers can provide an accurate integrated measure of energy expenditure in wild animals using many different locomotory modes.
accelerometer; dynamic body acceleration; field metabolic rate; muscle efficiency; seabird
Genetic and fossil data often lack the spatial and temporal precision for tracing the recent biogeographic history of species. Data with finer resolution are needed for studying distributional changes during modern human history. Here, I show that printed wormholes in rare books and artwork are trace fossils of wood-boring species with unusually accurate locations and dates. Analyses of wormholes printed in western Europe since the fifteenth century document the detailed biogeographic history of two putative species of invasive wood-boring beetles. Their distributions now overlap broadly, as an outcome of twentieth century globalization. However, the wormhole record revealed, unexpectedly, that their original ranges were contiguous and formed a stable line across central Europe, apparently a result of competition. Extension of the wormhole record, globally, will probably reveal other species and evolutionary insights. These data also provide evidence for historians in determining the place of origin or movement of a woodblock, book, document or art print.
evolution; biogeography; invasive species; wood-borer; art; Renaissance
Ectoparasites can reduce individual fitness by negatively affecting behavioural, morphological and physiological traits. In fishes, there are potential costs if ectoparasites decrease streamlining, thereby directly compromising swimming performance. Few studies have examined the effects of ectoparasites on fish swimming performance and none distinguish between energetic costs imposed by changes in streamlining and effects on host physiology. The bridled monocle bream (Scolopsis bilineatus) is parasitized by an isopod (Anilocra nemipteri), which attaches above the eye. We show that parasitized fish have higher standard metabolic rates (SMRs), poorer aerobic capacities and lower maximum swimming speeds than non-parasitized fish. Adding a model parasite did not affect SMR, but reduced maximum swimming speed and elevated oxygen consumption rates at high speeds to levels observed in naturally parasitized fish. This demonstrates that ectoparasites create drag effects that are important at high speeds. The higher SMR of naturally parasitized fish does, however, reveal an effect of parasitism on host physiology. This effect was easily reversed: fish whose parasite was removed 24 h earlier did not differ from unparasitized fish in any performance metrics. In sum, the main cost of this ectoparasite is probably its direct effect on streamlining, reducing swimming performance at high speeds.
respirometry; isopod; aerobic capacity; metabolic rate; critical swimming speed; drag
Birds are known to respond to nest-dwelling parasites by altering behaviours. Some bird species, for example, bring fresh plants to the nest, which contain volatile compounds that repel parasites. There is evidence that some birds living in cities incorporate cigarette butts into their nests, but the effect (if any) of this behaviour remains unclear. Butts from smoked cigarettes retain substantial amounts of nicotine and other compounds that may also act as arthropod repellents. We provide the first evidence that smoked cigarette butts may function as a parasite repellent in urban bird nests. The amount of cellulose acetate from butts in nests of two widely distributed urban birds was negatively associated with the number of nest-dwelling parasites. Moreover, when parasites were attracted to heat traps containing smoked or non-smoked cigarette butts, fewer parasites reached the former, presumably due to the presence of nicotine. Because urbanization changes the abundance and type of resources upon which birds depend, including nesting materials and plants involved in self-medication, our results are consistent with the view that urbanization imposes new challenges on birds that are dealt with using adaptations evolved elsewhere.
urban birds; nicotine; antiparasite defence; nest parasites; self-medication
The refugial speciation model, or ‘species pump’, is widely accepted in the context of tropical biogeography and has been advocated as an explanation for present species distributions in tropical Western and Central Africa. In order to test this hypothesis, a phylogeny of the cryptic arachnid order Ricinulei, based on four nuclear and mitochondrial DNA markers, was inferred. This ancient clade of litter-dwelling arthropods, endemic to the primary forests of Western and Central Africa and the Neotropics, might provide insights into the mode and tempo of evolution in Africa. Twenty-six African ricinuleid specimens were sampled from eight countries spanning the distribution of Ricinulei on the continent, and analysed together with Neotropical samples plus other arachnid outgroups. The phylogenetic and molecular dating results suggest that Ricinulei diversified in association with the fragmentation of Gondwana. The early diversification of Ricinoides in Western and Central Africa around 88 (±33) Ma fits old palaeogeographical events better than recent climatic fluctuations. Unlike most recent molecular studies, these results agree with fossil evidence, suggesting that refugia may have acted as ‘museums’ conserving ancient diversity rather than as engines generating diversity during successive episodes of climatic fluctuation in Africa.
Africa; refugia; marine incursion; Arachnida; Ricinulei; biogeography
Recent decades have seen a significant rise in studies in which evolution is observed and analysed directly—as it happens—under replicated, controlled conditions. Such ‘experimental evolution’ approaches offer a degree of resolution of evolutionary processes and their underlying genetics that is difficult or even impossible to achieve in more traditional comparative and retrospective analyses. In principle, experimental populations can be monitored for phenotypic and genetic changes with any desired level of replication and measurement precision, facilitating progress on fundamental and previously unresolved questions in evolutionary biology. Here, we summarize 10 invited papers in which experimental evolution is making significant progress on a variety of fundamental questions. We conclude by briefly considering future directions in this very active field of research, emphasizing the importance of quantitative tests of theories and the emerging role of genome-wide re-sequencing.
fitness; adaptation; epistasis; competition; social evolution
The role of predators in food webs extends beyond their ability to kill and consume prey. Such trait-mediated effects occur when signals of the predator influence the behaviour of other animals. Because all spiders are silk-producing carnivores, we hypothesized that silk alone would signal other arthropods and enhance non-lethal effects of spiders. We quantified the herbivory inflicted by two beetle species on green bean plants (Phaseolus vulgaris) in the presence of silkworm silk and spider silk along with no silk controls. Single leaflets were treated and enclosed with herbivores in the laboratory and field. Another set of leaflets were treated and left to experience natural herbivory in the field. Entire plants in the field were treated with silk and enclosed with herbivores or left exposed to herbivory. In all cases, the lowest levels of herbivory occurred with spider silk treatments and, in general, silkworm silk produced intermediate levels of leaf damage. These results suggest that silk may be a mechanism for the trait-mediated impacts of spiders and that it might contribute to integrated pest management programmes.
silk; spider; herbivory; trait-mediated effects; food web; non-consumptive effects
The rise of dinosaurs was a major event in vertebrate history, but the timing of the origin and early diversification of the group remain poorly constrained. Here, we describe Nyasasaurus parringtoni gen. et sp. nov., which is identified as either the earliest known member of, or the sister–taxon to, Dinosauria. Nyasasaurus possesses a unique combination of dinosaur character states and an elevated growth rate similar to that of definitive early dinosaurs. It demonstrates that the initial dinosaur radiation occurred over a longer timescale than previously thought (possibly 15 Myr earlier), and that dinosaurs and their immediate relatives are better understood as part of a larger Middle Triassic archosauriform radiation. The African provenance of Nyasasaurus supports a southern Pangaean origin for Dinosauria.
Dinosauria; Archosaur radiation; Triassic; Manda beds; phylogeny
The terminal respiratory units of the gas exchange tissue of the avian lung, the air capillaries (ACs) and the blood capillaries (BCs), are small and rigid: the basis of this mechanical feature has been highly contentious. Because the strength of the blood-gas barrier (BGB) of the mammalian lung has been attributed to the presence of type-IV collagen (T-IVc), localization of T-IVc in the basement membranes (BM) of the BGB and the epithelial–epithelial cell connections (E-ECCs) of the exchange tissue of the lung of the avian (chicken) lung was performed in order to determine whether it may likewise contribute to the strength of the BGB. T-IVc was localized in both the BM and the E-ECCs. As part of an integrated fibroskeletal scaffold on the lung, T-IVc may directly contribute to the strengths of the ACs and the BCs.
type-IV collagen; avian lung; air capillaries; blood capillaries; basement membrane; immuno-electron microscopy
One of the most mysterious aspects of insect clock mechanisms is that some insects, including Hymenoptera and Tribolium, only express a vertebrate-type cryptochrome (cry2). It is unknown whether or not cry2 underwent adaptive evolution in these insects. In the present study, we cloned and sequenced the full-length cry2 from a fig pollinator species, Ceratosolen solmsi (Hymenoptera: Chalcidoidea: Agaonidae), and examined the molecular evolution and daily expression of this gene. Our results suggest that cry2 underwent positive selection in the branch leading to hymenopteran insects. The function of CRY2 might have been fixed since undergoing natural selection in the ancestor of Hymenoptera. Male pollinators showed stronger rhythmicity in the host figs, which reflect an adaptation to their life cycles.
fig pollinator; cryptochrome; adaptation; positive selection
Bacterial populations in clinical and laboratory settings contain a significant proportion of mutants with elevated mutation rates (mutators). Mutators have a particular advantage when multiple beneficial mutations are needed for fitness, as in antibiotic resistance. Nevertheless, high mutation rates potentially lead to increasing numbers of deleterious mutations and subsequently to the decreased fitness of mutators. To test how fitness changed with mutation accumulation, genome sequencing and fitness assays of nine Escherichia coli mutY mutators were undertaken in an evolving chemostat population at three time points. Unexpectedly, the fitness in members of the mutator subpopulation became constant despite a growing number of mutations over time. To test if the accumulated mutations affected fitness, we replaced each of the known beneficial mutations with wild-type alleles in a mutator isolate. We found that the other 25 accumulated mutations were not deleterious. Our results suggest that isolates with deleterious mutations are eliminated by competition in a continuous culture, leaving mutators with mostly neutral mutations. Interestingly, the mutator–non-mutator balance in the population reversed after the fitness plateau of mutators was reached, suggesting that the mutator–non-mutator ratio in populations has more to do with competition between members of the population than the accumulation of deleterious mutations.
bacterial genomics; experimental evolution; mutators
The extreme body size of blue whales requires a high energy intake and therefore demands efficient foraging strategies. As an obligate lunge feeder on aggregations of small zooplankton, blue whales engulf a large volume of prey-laden water in a single, rapid gulp. The efficiency of this feeding mechanism is strongly dependent on the amount of prey that can be captured during each lunge, yet food resources tend to be patchily distributed in both space and time. Here, we measured the three-dimensional kinematics and foraging behaviour of blue whales feeding on krill, using suction-cup attached multi-sensor tags. Our analyses revealed 360° rolling lunge-feeding manoeuvres that reorient the body and position the lower jaws so that a krill patch can be engulfed with the whale's body inverted. We also recorded these rolling behaviours when whales were in a searching mode in between lunges, suggesting that this behaviour also enables the whale to visually process the prey field and maximize foraging efficiency by surveying for the densest prey aggregations. These results reveal the complex manoeuvrability that is required for large rorqual whales to exploit prey patches and highlight the need to fully understand the three-dimensional interactions between predator and prey in the natural environment.
Mysticeti; manoeuvrability; foraging
The island rule, a pattern of size shifts on islands, is an oft-cited but little understood phenomenon of evolutionary biology. Here, we explore the evolutionary mechanisms behind the rule in 184 mammal species, testing climatic, ecological and phylogenetic hypotheses in a robust quantitative framework. Our findings confirm the importance of species’ ecological traits in determining both the strength and the direction of body size changes on islands. Although the island rule pattern appears relatively weak overall, we find strongest support for models incorporating trait, climatic and geographical factors in a phylogenetic context, lending support to the idea that the island rule is a complex phenomenon driven by interacting intrinsic and extrinsic mechanisms. Overall, we find that different clades may be evolutionarily predisposed to dwarfism or gigantism, but the magnitude of size changes depends more on adaptation to the novel island environment.
island rule; body size; mammal; niche; morphology; climate