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2.  Spatial memory: are lizards really deficient? 
Biology Letters  2012;8(6):939-941.
In many animals, behaviours such as territoriality, mate guarding, navigation and food acquisition rely heavily on spatial memory abilities; this has been demonstrated in diverse taxa, from invertebrates to mammals. However, spatial memory ability in squamate reptiles has been seen as possible, at best, or non-existent, at worst. Of the few previous studies testing for spatial memory in squamates, some have found no evidence of spatial memory while two studies have found evidence of spatial memory in snakes, but have been criticized based on methodological issues. We used the Barnes maze, a common paradigm to test spatial memory abilities in mammals, to test for spatial memory abilities in the side-blotched lizard (Uta stansburiana). We found the existence of spatial memory in this species using this spatial task. Thus, our study supports the existence of spatial memory in this squamate reptile species and seeks to parsimoniously align this species with the diverse taxa that demonstrate spatial memory ability.
PMCID: PMC3497115  PMID: 22933038
cognition; lizards; spatial memory; Uta stansburiana
3.  Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage 
Biology Letters  2012;8(6):1028-1031.
The turtle shell and the relationship of the shoulder girdle inside or ‘deep’ to the ribcage have puzzled neontologists and developmental biologists for more than a century. Recent developmental and fossil data indicate that the shoulder girdle indeed lies inside the shell, but anterior to the ribcage. Developmental biologists compare this orientation to that found in the model organisms mice and chickens, whose scapula lies laterally on top of the ribcage. We analyse the topological relationship of the shoulder girdle relative to the ribcage within a broader phylogenetic context and determine that the condition found in turtles is also found in amphibians, monotreme mammals and lepidosaurs. A vertical scapula anterior to the thoracic ribcage is therefore inferred to be the basal amniote condition and indicates that the condition found in therian mammals and archosaurs (which includes both developmental model organisms: chickens and mice) is derived and not appropriate for studying the developmental origin of the turtle shell. Instead, among amniotes, either monotreme mammals or lepidosaurs should be used.
PMCID: PMC3497105  PMID: 22809725
evolution and development; turtle shell; evolutionary novelty; Odontochelys semitestacea
4.  Towards a general life-history model of the superorganism: predicting the survival, growth and reproduction of ant societies 
Biology Letters  2012;8(6):1059-1062.
Social insect societies dominate many terrestrial ecosystems across the planet. Colony members cooperate to capture and use resources to maximize survival and reproduction. Yet, when compared with solitary organisms, we understand relatively little about the factors responsible for differences in the rates of survival, growth and reproduction among colonies. To explain these differences, we present a mathematical model that predicts these three rates for ant colonies based on the body sizes and metabolic rates of colony members. Specifically, the model predicts that smaller colonies tend to use more energy per gram of biomass, live faster and die younger. Model predictions are supported with data from whole colonies for a diversity of species, with much of the variation in colony-level life history explained based on physiological traits of individual ants. The theory and data presented here provide a first step towards a more general theory of colony life history that applies across species and environments.
PMCID: PMC3497106  PMID: 22896271
ant colony; life history; metabolic scaling
5.  Migratory constraints on yolk precursors limit yolk androgen deposition and underlie a brood reduction strategy in rockhopper penguins 
Biology Letters  2012;8(6):1055-1058.
Hormonally mediated maternal effects link maternal phenotype and environmental conditions to offspring phenotype. The production of lipid-rich maternal yolk precursors may provide a mechanism by which lipophilic steroid hormones can be transported to developing yolks, thus predicting a positive correlation between yolk precursors in mothers and androgen levels in eggs. Using rockhopper penguins (Eudyptes chrysocome), which produce a two-egg clutch characterized by extreme egg-size dimorphism, reversed hatching asynchrony and brood-reduction, we examined correlations between circulating concentrations of the primary yolk-precursor vitellogenin (VTG) and levels of yolk androgens. Previous work in Eudyptes penguins has shown that egg-size dimorphism is the product of migratory constraints on yolk precursor production. We predicted that if yolk precursors are constrained, androgen transport to developing yolks would be similarly constrained. We reveal positive linear relationships between maternal VTG and androgens in small A-eggs but not larger B-eggs, which is consistent with a migratory constraint operating on the A-egg. Results suggest that intra-clutch variation in total yolk androgen levels depends on the production and uptake of yolk precursors. The brood reduction strategy common to Eudyptes might thus be best described as the result of a migratory constraint.
PMCID: PMC3497107  PMID: 22809718
androstenedione; testosterone; physiological epiphenomenon hypothesis; vitellogenin; maternal effects; carryover effects
6.  Testing microstructural adaptation in the earliest dental tools 
Biology Letters  2012;8(6):952-955.
Conodont elements are the earliest vertebrate dental structures. The dental tools on elements responsible for food fracture—cusps and denticles—are usually composed of lamellar crown tissue (a putative enamel homologue) and the enigmatic tissue known as ‘white matter’. White matter is unique to conodonts and has been hypothesized to be a functional adaptation for the use of elements as teeth. We test this quantitatively using finite-element analysis. Our results indicate that white matter allowed cusps and denticles to withstand greater tensile stresses than do cusps comprised solely of lamellar crown tissue. Microstructural variation is demonstrably associated with dietary and loading differences in teeth, so secondary loss of white matter through conodont phylogeny may reflect changes in diet and element occlusal kinematics. The presence, development and distribution of white matter could thus provide constraints on function in the first vertebrate dental structures.
PMCID: PMC3497108  PMID: 22764115
finite-element analysis; conodont; white matter; teeth
7.  Social familiarity modulates personality trait in a cichlid fish 
Biology Letters  2012;8(6):936-938.
Personality traits, such as exploration–avoidance, are expected to be adaptive in a given context (e.g. low-risk environment) but to be maladaptive in others (e.g. high-risk environment). Therefore, it is expected that personality traits are flexible and respond to environmental fluctuations, given that consistency across different contexts is maintained, so that the relative individual responses in relation to others remains the same (i.e. although the magnitude of the response varies the differences between high and low responders are kept). Here, we tested the response of male cichlid fish (Oreochromis mossambicus) to a novel object (NO) in three different social contexts: (i) social isolation, (ii) in the presence of an unfamiliar conspecific, and (iii) in the presence of a familiar conspecific. Males in the familiar treatment exhibited more exploratory behaviour and less neophobia than males in either the unfamiliar or the social isolation treatments. However, there were no overall correlations in individual behaviour across the three treatments, suggesting a lack of consistency in exploration–avoidance as measured by the NO test in this species. Moreover, there were no differences in cortisol responsiveness to an acute stressor between the three treatments. Together, these results illustrate how behavioural traits usually taken as measures of personality may exhibit significant flexibility and lack the expected consistency across different social contexts.
PMCID: PMC3497109  PMID: 22859562
exploratory behaviour; neophobia; boldness; personality; phenotypic plasticity; stress
9.  Theft in an ultimatum game: chimpanzees and bonobos are insensitive to unfairness 
Biology Letters  2012;8(6):942-945.
Humans, but not chimpanzees, punish unfair offers in ultimatum games, suggesting that fairness concerns evolved sometime after the split between the lineages that gave rise to Homo and Pan. However, nothing is known about fairness concerns in the other Pan species, bonobos. Furthermore, apes do not typically offer food to others, but they do react against theft. We presented a novel game, the ultimatum theft game, to both of our closest living relatives. Bonobos and chimpanzee ‘proposers’ consistently stole food from the responders' portions, but the responders did not reject any non-zero offer. These results support the interpretation that the human sense of fairness is a derived trait.
PMCID: PMC3497113  PMID: 22896269
inequity; fairness; ultimatum game; punishment; chimpanzees; bonobos
10.  Environmental variability and acoustic signals: a multi-level approach in songbirds 
Biology Letters  2012;8(6):928-931.
Among songbirds, growing evidence suggests that acoustic adaptation of song traits occurs in response to habitat features. Despite extensive study, most research supporting acoustic adaptation has only considered acoustic traits averaged for species or populations, overlooking intraindividual variation of song traits, which may facilitate effective communication in heterogeneous and variable environments. Fewer studies have explicitly incorporated sexual selection, which, if strong, may favour variation across environments. Here, we evaluate the prevalence of acoustic adaptation among 44 species of songbirds by determining how environmental variability and sexual selection intensity are associated with song variability (intraindividual and intraspecific) and short-term song complexity. We show that variability in precipitation can explain short-term song complexity among taxonomically diverse songbirds, and that precipitation seasonality and the intensity of sexual selection are related to intraindividual song variation. Our results link song complexity to environmental variability, something previously found for mockingbirds (Family Mimidae). Perhaps more importantly, our results illustrate that individual variation in song traits may be shaped by both environmental variability and strength of sexual selection.
PMCID: PMC3497114  PMID: 22859557
acoustic adaptation; birdsong; environmental variability; selection; sensory drive; song variation
11.  Proximity data-loggers increase the quantity and quality of social network data 
Biology Letters  2012;8(6):917-920.
Social network analysis is an ideal quantitative tool for advancing our understanding of complex social behaviour. However, this approach is often limited by the challenges of accurately characterizing social structure and measuring network heterogeneity. Technological advances have facilitated the study of social networks, but to date, all such work has focused on large vertebrates. Here, we provide proof of concept for using proximity data-logging to quantify the frequency of social interactions, construct weighted networks and characterize variation in the social behaviour of a lek-breeding bird, the wire-tailed manakin, Pipra filicauda. Our results highlight how this approach can ameliorate the challenges of social network data collection and analysis by concurrently improving data quality and quantity.
PMCID: PMC3497117  PMID: 22859558
coded nanotag; proximity data-loggers; social networks
12.  Northward range extension of an endemic soil decomposer with a distinct trophic position 
Biology Letters  2012;8(6):956-959.
Ecological niche theory asserts that invading species become established only if introduced propagules survive stochastic mortality and can exploit resources unconsumed by resident species. Because their transportation is not controlled by plant health or biosecurity regulations, soil macrofauna decomposers, including earthworms are probably introduced frequently into non-native soils. Yet even with climatic change, exotic earthworm species from southern Europe have not been reported to become established in previously glaciated areas of northern Europe that already have trophically differentiated earthworm communities of ‘peregrine’ species. We discovered established populations of the earthworm Prosellodrilus amplisetosus (Lumbricidae), a member of a genus endemic to southern France, in six habitats of an urban farm in Dublin, Ireland, about 1000 km north of the genus's endemic range. Not only was P. amplisetosus the dominant endogeic (geophagous) earthworm species in two habitats, it also occupied a significantly different trophic position from the resident species, as evinced by stable isotope ratio analysis. The suggested ability of this non-native species to feed on and assimilate isotopically more enriched soil carbon (C) and nitrogen fractions that are inaccessible to resident species portends potential implications of decomposer range expansions for soil functioning including C sequestration.
PMCID: PMC3497118  PMID: 22832130
decomposers; ecological niche; soil carbon; soil macrofauna; species introductions
13.  Fire creates host plant patches for monarch butterflies 
Biology Letters  2012;8(6):968-971.
Monarch butterflies (Danaus plexippus) depend on the presence of host plants (Asclepias spp.) within their breeding range for reproduction. In the southern Great Plains, Asclepias viridis is a perennial that flowers in May and June, and starts to senesce by August. It is locally abundant and readily used by monarchs as a host plant. We evaluated the effects of summer prescribed fire on A. viridis and the use of A. viridis by monarch butterflies. Summer prescribed fire generated a newly emergent population of A. viridis that was absent in other areas. Pre-migrant monarch butterflies laid eggs on A. viridis in summer burned plots in late August and September, allowing adequate time for a new generation of adult monarchs to emerge and migrate south to their overwintering grounds. Thus, summer prescribed fire may provide host plant patches and/or corridors for pre-migrant monarchs during a time when host plant availability may be limited in other areas.
PMCID: PMC3497119  PMID: 22859559
Asclepias viridis; Danaus plexippus; migration; milkweed; prescribed fire; reproduction
14.  Pro-sociality without empathy 
Biology Letters  2012;8(6):910-912.
Empathy, the capacity to recognize and share feelings experienced by another individual, is an important trait in humans, but is not the same as pro-sociality, the tendency to behave so as to benefit another individual. Given the importance of understanding empathy's evolutionary emergence, it is unsurprising that many studies attempt to find evidence for it in other species. To address the question of what should constitute evidence for empathy, we offer a critical comparison of two recent studies of rescuing behaviour that report similar phenomena but are interpreted very differently by their authors. In one of the studies, rescue behaviour in rats was interpreted as providing evidence for empathy, whereas in the other, rescue behaviour in ants was interpreted without reference to sharing of emotions. Evidence for empathy requires showing that actor individuals possess a representation of the receiver's emotional state and are driven by the psychological goal of improving its wellbeing. Proving psychological goal-directedness by current standards involves goal-devaluation and causal sensitivity protocols, which, in our view, have not been implemented in available publications. Empathy has profound significance not only for cognitive and behavioural sciences but also for philosophy and ethics and, in our view, remains unproven outside humans.
PMCID: PMC3497120  PMID: 22859561
empathy; pro-social behaviour; intentionality; goal-directedness
15.  Indirect commensalism promotes persistence of secondary consumer species 
Biology Letters  2012;8(6):960-963.
Local species extinctions may lead to, often unexpected, secondary extinctions. To predict these, we need to understand how indirect effects, within a network of interacting species, affect the ability of species to persist. It has been hypothesized that the persistence of some predators depends on other predator species that suppress competitively dominant prey to low levels, allowing a greater diversity of prey species, and their predators, to coexist. We show that, in experimental insect communities, the absence of one parasitoid wasp species does indeed lead to the extinction of another that is separated by four trophic links. These results highlight the importance of a holistic systems perspective to biodiversity conservation and the necessity to include indirect population dynamic effects in models for predicting cascading extinctions in networks of interacting species.
PMCID: PMC3497121  PMID: 22896268
aphids; indirect effects; food web; parasitoid; resource competition; secondary extinctions
16.  Evolutionary novelty in a rat with no molars 
Biology Letters  2012;8(6):990-993.
Rodents are important ecological components of virtually every terrestrial ecosystem. Their success is a result of their gnawing incisors, battery of grinding molars and diastema that spatially and functionally separates the incisors from the molars. Until now these traits defined all rodents. Here, we describe a new species and genus of shrew-rat from Sulawesi Island, Indonesia that is distinguished from all other rodents by the absence of cheek teeth. Moreover, rather than gnawing incisors, this animal has bicuspid upper incisors, also unique among the more than 2200 species of rodents. Stomach contents from a single specimen suggest that the species consumes only earthworms. We posit that by specializing on soft-bodied prey, this species has had no need to process food by chewing, allowing its dentition to evolve for the sole purpose of procuring food. Thus, the removal of functional constraints, often considered a source of evolutionary innovations, may also lead to the loss of the very same traits that fuelled evolutionary diversification in the past.
PMCID: PMC3497122  PMID: 22915626
convergence; key innovation; new species; shrew-rat; Sulawesi; vermivory
17.  Intralocus sexual conflict over human height 
Biology Letters  2012;8(6):976-978.
Intralocus sexual conflict (IASC) occurs when a trait under selection in one sex constrains the other sex from achieving its sex-specific fitness optimum. Selection pressures on body size often differ between the sexes across many species, including humans: among men individuals of average height enjoy the highest reproductive success, while shorter women have the highest reproductive success. Given its high heritability, IASC over human height is likely. Using data from sibling pairs from the Wisconsin Longitudinal Study, we present evidence for IASC over height: in shorter sibling pairs (relatively) more reproductive success (number of children) was obtained through the sister than through the brother of the sibling pair. By contrast, in average height sibling pairs most reproductive success was obtained through the brother relative to the sister. In conclusion, we show that IASC over a heritable, sexually dimorphic physical trait (human height) affects Darwinian fitness in a contemporary human population.
PMCID: PMC3497124  PMID: 22875819
stature; sexual antagonism; reproductive success; genetic conflict
18.  Increased aggression during human group contests when competitive ability is more similar 
Biology Letters  2012;8(6):921-923.
Theoretical analyses and empirical studies have revealed that conflict escalation is more likely when individuals are more similar in resource-holding potential (RHP). Conflicts can also occur between groups, but it is unknown whether conflicts also escalate more when groups are more similar in RHP. We tested this hypothesis in humans, using data from two professional sports competitions: football (the Bundesliga, the German first division of football) and basketball (the NBA, the North American National Basketball Association). We defined RHP based on the league ranks of the teams involved in the competition (i.e. their competitive ability) and measured conflict escalation by the number of fouls committed. We found that in both sports the number of fouls committed increased when the difference in RHP was smaller. Thus, we provide what is to our best knowledge the first evidence that, as in conflicts between individuals, conflicts escalate more when groups are more similar in RHP.
PMCID: PMC3497125  PMID: 22896272
resource-holding potential; aggression; group competition; human sports
19.  Metabolic effects of CO2 anaesthesia in Drosophila melanogaster 
Biology Letters  2012;8(6):1050-1054.
Immobilization of insects is necessary for various experimental purposes, and CO2 exposure remains the most popular anaesthetic method in entomological research. A number of negative side effects of CO2 anaesthesia have been reported, but CO2 probably brings about metabolic modifications that are poorly known. In this work, we used GC/MS-based metabolic fingerprinting to assess the effect of CO2 anaesthesia in Drosophila melanogaster adults. We analysed metabolic variation of flies submitted to acute CO2 exposure and assessed the temporal metabolic changes during short- and long-term recovery. We found that D. melanogaster metabotypes were significantly affected by the anaesthetic treatment. Metabolic changes caused by acute CO2 exposure were still manifested after 14 h of recovery. However, we found no evidence of metabolic alterations when a long recovery period was allowed (more than 24 h). This study points to some metabolic pathways altered during CO2 anaesthesia (e.g. energetic metabolism). Evidence of short-term metabolic changes indicates that CO2 anaesthesia should be used with utmost caution in physiological studies when a short recovery is allowed. In spite of this, CO2 treatment seems to be an acceptable anaesthetic method provided that a long recovery period is allowed (more than 24 h).
PMCID: PMC3497127  PMID: 22915627
Drosophila; anaesthesia; GC–MS; metabolic fingerprinting; recovery
21.  The consequences of climate change at an avian influenza ‘hotspot’ 
Biology Letters  2012;8(6):1036-1039.
Avian influenza viruses (AIVs) pose significant danger to human health. A key step in managing this threat is understanding the maintenance of AIVs in wild birds, their natural reservoir. Ruddy turnstones (Arenaria interpres) are an atypical bird species in this regard, annually experiencing high AIV prevalence in only one location—Delaware Bay, USA, during their spring migration. While there, they congregate on beaches, attracted by the super-abundance of horseshoe crab eggs. A relationship between ruddy turnstone and horseshoe crab (Limulus polyphemus) population sizes has been established, with a declining horseshoe crab population linked to a corresponding drop in ruddy turnstone population sizes. The effect of this interaction on AIV prevalence in ruddy turnstones has also been addressed. Here, we employ a transmission model to investigate how the interaction between these two species is likely to be altered by climate change. We explore the consequences of this modified interaction on both ruddy turnstone population size and AIV prevalence and show that, if climate change leads to a large enough mismatch in species phenology, AIV prevalence in ruddy turnstones will increase even as their population size decreases.
PMCID: PMC3497130  PMID: 22933039
avian influenza virus; Delaware Bay; climate change; transmission model
22.  Evidence that gestation duration and lactation duration are coupled traits in primates 
Biology Letters  2012;8(6):998-1001.
Gestation duration and lactation duration are usually treated as independently evolving traits in primates, but the metabolic theory of ecology (MTE) suggests both durations should be determined by metabolic rate. We used phylogenetic generalized least-squares linear regression to test these different perspectives. We found that the allometries of the durations are divergent from each other and different from the scaling exponent predicted by the MTE (0.25). Gestation duration increases much more slowly (0.06 < m < 0.12), and lactation duration much more quickly (0.36 < m < 0.52) with body mass than the MTE predicts. By contrast, we found that the combined duration of gestation and lactation is consistent with the MTE's predictions (0.22 < m < 0.35). These results suggest that gestation duration and lactation duration might best be viewed as distinct but coupled adaptations. When transferring energy to their offspring, primate mothers must meet metabolically dictated physiological requirements while optimizing the timing of the switch from gestation to lactation in relation to some as-yet-unidentified body-size-related factor.
PMCID: PMC3497131  PMID: 22915631
allometry; constraint; energy transfer; metabolic theory of ecology
23.  Evolution of gliding in Southeast Asian geckos and other vertebrates is temporally congruent with dipterocarp forest development 
Biology Letters  2012;8(6):994-997.
Gliding morphologies occur in diverse vertebrate lineages in Southeast Asian rainforests, including three gecko genera, plus frogs, snakes, agamid lizards and squirrels. It has been hypothesized that repeated evolution of gliding is related to the dominance of Asian rainforest tree floras by dipterocarps. For dipterocarps to have influenced the evolution of gliding in Southeast Asian vertebrates, gliding lineages must have Eocene or later origins. However, divergence times are not known for most lineages. To investigate the temporal pattern of Asian gliding vertebrate evolution, we performed phylogenetic and molecular clock analyses. New sequence data for geckos incorporate exemplars of each gliding genus (Cosymbotus, Luperosaurus and Ptychozoon), whereas analyses of other vertebrate lineages use existing sequence data. Stem ages of most gliding vertebrates, including all geckos, cluster in the time period when dipterocarps came to dominate Asian tropical forests. These results demonstrate that a gliding/dipterocarp correlation is temporally viable, and caution against the assumption of early origins for apomorphic taxa.
PMCID: PMC3497132  PMID: 22977067
volant; parachuting; Sundaland; phylogeny; Reptilia; Mammalia
24.  Causes of hatching failure in endangered birds 
Biology Letters  2012;8(6):964-967.
About 10 per cent of birds' eggs fail to hatch, but the incidence of failure can be much higher in endangered species. Most studies fail to distinguish between infertility (due to a lack of sperm) and embryo mortality as the cause of hatching failure, yet doing so is crucial in order to understand the underlying problem. Using newly validated techniques to visualize sperm and embryonic tissue, we assessed the fertility status of unhatched eggs of five endangered species, including both wild and captive birds. All eggs were classified as ‘infertile’ when collected, but most were actually fertile with numerous sperm on the ovum. Eggs of captive birds had fewer sperm and were more likely to be infertile than those of wild birds. Our findings raise important questions regarding the management of captive breeding programmes.
PMCID: PMC3497133  PMID: 22977070
helmeted honeyeater; hihi; captive breeding; orange-bellied parrot; Spix's macaw; yellow-shouldered Amazon parrot
25.  Cone monochromacy and visual pigment spectral tuning in wobbegong sharks 
Biology Letters  2012;8(6):1019-1022.
Much is known regarding the evolution of colour vision in nearly every vertebrate class, with the notable exception of the elasmobranchs. While multiple spectrally distinct cone types are found in some rays, sharks appear to possess only a single class of cone and, therefore, may be colour blind. In this study, the visual opsin genes of two wobbegong species, Orectolobus maculatus and Orectolobus ornatus, were isolated to verify the molecular basis of their monochromacy. In both species, only two opsin genes are present, RH1 (rod) and LWS (cone), which provide further evidence to support the concept that sharks possess only a single cone type. Examination of the coding sequences revealed substitutions that account for interspecific variation in the photopigment absorbance spectra, which may reflect the difference in visual ecology between these species.
PMCID: PMC3497134  PMID: 22993239
shark; monochromacy; opsin; rod; cone

Results 1-25 (173)