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1.  Experimental perspective on fallback foods and dietary adaptations in early hominins 
Biology Letters  2014;10(1):20130789.
The robust jaws and large, thick-enameled molars of the Plio–Pleistocene hominins Australopithecus and Paranthropus have long been interpreted as adaptations for hard-object feeding. Recent studies of dental microwear indicate that only Paranthropus robustus regularly ate hard items, suggesting that the dentognathic anatomy of other australopiths reflects rare, seasonal exploitation of hard fallback foods. Here, we show that hard-object feeding cannot explain the extreme morphology of Paranthropus boisei. Rather, analysis of long-term dietary plasticity in an animal model suggests year-round reliance on tough foods requiring prolonged postcanine processing in P. boisei. Increased consumption of such items may have marked the earlier transition from Ardipithecus to Australopithecus, with routine hard-object feeding in P. robustus representing a novel behaviour.
PMCID: PMC3917327  PMID: 24402713
australopiths; masticatory apparatus; phenotypic plasticity
2.  Hunter–gatherers have less famine than agriculturalists 
Biology Letters  2014;10(1):20130853.
The idea that hunter–gatherer societies experience more frequent famine than societies with other modes of subsistence is pervasive in the literature on human evolution. This idea underpins, for example, the ‘thrifty genotype hypothesis’. This hypothesis proposes that our hunter–gatherer ancestors were adapted to frequent famines, and that these once adaptive ‘thrifty genotypes’ are now responsible for the current obesity epidemic. The suggestion that hunter–gatherers are more prone to famine also underlies the widespread assumption that these societies live in marginal habitats. Despite the ubiquity of references to ‘feast and famine’ in the literature describing our hunter–gatherer ancestors, it has rarely been tested whether hunter–gatherers suffer from more famine than other societies. Here, we analyse famine frequency and severity in a large cross-cultural database, in order to explore relationships between subsistence and famine risk. This is the first study to report that, if we control for habitat quality, hunter–gatherers actually had significantly less—not more—famine than other subsistence modes. This finding challenges some of the assumptions underlying for models of the evolution of the human diet, as well as our understanding of the recent epidemic of obesity and type 2 diabetes mellitus.
PMCID: PMC3917328  PMID: 24402714
food shortages; foragers; palaeodiet; obesity
3.  The corn snake yolk sac becomes a solid tissue filled with blood vessels and yolk-rich endodermal cells 
Biology Letters  2014;10(1):20130870.
The amniote egg was a key innovation in vertebrate evolution because it supports an independent existence in terrestrial environments. The egg is provisioned with yolk, and development depends on the yolk sac for the mobilization of nutrients. We have examined the yolk sac of the corn snake Pantherophis guttatus by the dissection of living eggs. In contrast to the familiar fluid-filled sac of birds, the corn snake yolk sac invades the yolk mass to become a solid tissue. There is extensive proliferation of yolk-filled endodermal cells, which associate with a meshwork of blood vessels. These novel attributes of the yolk sac of corn snakes compared with birds suggest new pathways for the evolution of the amniote egg.
PMCID: PMC3917329  PMID: 24402715
amniote egg; yolk sac; corn snake; endoderm
4.  Migration and stress during reproduction govern telomere dynamics in a seabird 
Biology Letters  2014;10(1):20130889.
Changes in telomere length are believed to reflect changes in physiological state and life expectancy in animals. However, much remains unknown about the determinants of telomere dynamics in wild populations, and specifically the influence of conditions during highly mobile life-history stages, for example migration. We tested whether telomere dynamics were associated with migratory behaviour and/or with stress during reproduction in free-living seabirds. We induced short-term stress during reproduction in chick-rearing, black-legged kittiwakes (Rissa tridactyla), tracked winter migration with geolocators and measured telomere length before and after winter migration. We found that time spent at wintering grounds correlated with reduced telomere loss, while stress during reproduction accelerated telomere shortening. Our results suggest that different life-history stages interact to influence telomere length, and that migratory patterns may be important determinants of variation in an individual's telomere dynamics.
PMCID: PMC3917333  PMID: 24429681
overwintering; migratory behaviour; breeding; seasonal effects; carry-over; telomeres
5.  Salmon lice increase the age of returning Atlantic salmon 
Biology Letters  2014;10(1):20130896.
The global increase in the production of domestic farmed fish in open net pens has created concerns about the resilience of wild populations owing to shifts in host–parasite systems in coastal ecosystems. However, little is known about the effects of increased parasite abundance on life-history traits in wild fish populations. Here, we report the results of two separate studies in which 379 779 hatchery-reared Atlantic salmon smolts were treated (or not) against salmon lice, marked and released. Adults were later recaptured, and we specifically tested whether the age distribution of the returning spawners was affected by the treatment. The estimates of parasite-induced mortality were 31.9% and 0.6% in the River Vosso and River Dale stock experiments, respectively. Age of returning salmon was on average higher in treated versus untreated fish. The percentages of fish returning after one winter at sea were 37.5% and 29.9% for the treated and untreated groups, respectively. We conclude that salmon lice increase the age of returning salmon, either by affecting their age at maturity or by disproportionately increasing mortality in fish that mature early.
PMCID: PMC3917334  PMID: 24478199
age-at-maturation; sea lice; salmon; life-history traits
6.  Rewards and the evolution of cooperation in public good games 
Biology Letters  2014;10(1):20130903.
Properly coordinating cooperation is relevant for resolving public good problems, such as clean energy and environmental protection. However, little is known about how individuals can coordinate themselves for a certain level of cooperation in large populations of strangers. In a typical situation, a consensus-building process rarely succeeds, owing to a lack of face and standing. The evolution of cooperation in this type of situation is studied here using threshold public good games, in which cooperation prevails when it is initially sufficient, or otherwise it perishes. While punishment is a powerful tool for shaping human behaviours, institutional punishment is often too costly to start with only a few contributors, which is another coordination problem. Here, we show that whatever the initial conditions, reward funds based on voluntary contribution can evolve. The voluntary reward paves the way for effectively overcoming the coordination problem and efficiently transforms freeloaders into cooperators with a perceived small risk of collective failure.
PMCID: PMC3917335  PMID: 24478200
public good game; evolution of cooperation; reward; punishment; coordination problem
7.  Humans rely on the same rules to assess emotional valence and intensity in conspecific and dog vocalizations 
Biology Letters  2014;10(1):20130926.
Humans excel at assessing conspecific emotional valence and intensity, based solely on non-verbal vocal bursts that are also common in other mammals. It is not known, however, whether human listeners rely on similar acoustic cues to assess emotional content in conspecific and heterospecific vocalizations, and which acoustical parameters affect their performance. Here, for the first time, we directly compared the emotional valence and intensity perception of dog and human non-verbal vocalizations. We revealed similar relationships between acoustic features and emotional valence and intensity ratings of human and dog vocalizations: those with shorter call lengths were rated as more positive, whereas those with a higher pitch were rated as more intense. Our findings demonstrate that humans rate conspecific emotional vocalizations along basic acoustic rules, and that they apply similar rules when processing dog vocal expressions. This suggests that humans may utilize similar mental mechanisms for recognizing human and heterospecific vocal emotions.
PMCID: PMC3917336  PMID: 24402716
dog; human; vocal communication; emotion valence assessment; emotion intensity assessment; non-verbal emotion expressions
8.  Natural selection can favour ‘irrational’ behaviour 
Biology Letters  2014;10(1):20130935.
Understanding decisions is the fundamental aim of the behavioural sciences. The theory of rational choice is based on axiomatic principles such as transitivity and independence of irrelevant alternatives (IIA). Empirical studies have demonstrated that the behaviour of humans and other animals often seems irrational; there can be a lack of transitivity in choice and seemingly irrelevant alternatives can alter decisions. These violations of transitivity and IIA undermine rational choice theory. However, we show that an individual that is maximizing its rate of food gain can exhibit failure of transitivity and IIA. We show that such violations can be caused because a current option may disappear in the near future or a better option may reappear soon. Current food options can be indicative of food availability in the near future, and this key feature can result in apparently irrational behaviour.
PMCID: PMC3917337  PMID: 24429682
rate maximization; transitivity; independence of irrelevant alternatives; rationality; decision-making
9.  No universal scale-dependent impacts of invasive species on native plant species richness 
Biology Letters  2014;10(1):20130939.
A growing number of studies seeking generalizations about the impact of plant invasions compare heavily invaded sites to uninvaded sites. But does this approach warrant any generalizations? Using two large datasets from forests, grasslands and desert ecosystems across the conterminous United States, we show that (i) a continuum of invasion impacts exists in many biomes and (ii) many possible species–area relationships may emerge reflecting a wide range of patterns of co-occurrence of native and alien plant species. Our results contradict a smaller recent study by Powell et al. 2013 (Science 339, 316–318. (doi:10.1126/science.1226817)), who compared heavily invaded and uninvaded sites in three biomes and concluded that plant communities invaded by non-native plant species generally have lower local richness (intercepts of log species richness–log area regression lines) but steeper species accumulation with increasing area (slopes of the regression lines) than do uninvaded communities. We conclude that the impacts of plant invasions on plant species richness are not universal.
PMCID: PMC3917338  PMID: 24478201
species–area relationships; alien species; native species; alien species impacts
10.  Are thyroid hormones mediators of incubation temperature-induced phenotypes in birds? 
Biology Letters  2014;10(1):20130950.
Incubation temperature influences a suite of traits in avian offspring. However, the mechanisms underlying expression of these phenotypes are unknown. Given the importance of thyroid hormones in orchestrating developmental processes, we hypothesized that they may act as an upstream mechanism mediating the effects of temperature on hatchling phenotypic traits such as growth and thermoregulation. We found that plasma T3, but not T4 concentrations, differed among newly hatched wood ducks (Aix sponsa) from different embryonic incubation temperatures. T4 at hatching correlated with time spent hatching, and T3 correlated with hatchling body condition, tarsus length, time spent hatching and incubation period. In addition, the T3 : T4 ratio differed among incubation temperatures at hatch. Our findings are consistent with the hypothesis that incubation temperature modulates plasma thyroid hormones which in turn influences multiple aspects of duckling phenotype.
PMCID: PMC3917339  PMID: 24402717
maternal effects; parental care; triiodothyronine
11.  Singing in the moonlight: dawn song performance of a diurnal bird varies with lunar phase 
Biology Letters  2014;10(1):20130970.
It is well established that the lunar cycle can affect the behaviour of nocturnal animals, but its potential to have a similar influence on diurnal species has received less research attention. Here, we demonstrate that the dawn song of a cooperative songbird, the white-browed sparrow weaver (Plocepasser mahali), varies with moon phase. When the moon was above the horizon at dawn, males began singing on average 10 min earlier, if there was a full moon compared with a new moon, resulting in a 67% mean increase in performance period and greater total song output. The lack of a difference between full and new moon dawns when the moon was below the horizon suggests that the observed effects were driven by light intensity, rather than driven by other factors associated with moon phase. Effects of the lunar cycle on twilight signalling behaviour have implications for both pure and applied animal communication research.
PMCID: PMC3917340  PMID: 24429683
lunar cycle; moon phase; twilight; light pollution; song; dawn chorus
12.  Sideways walking: preferred is slow, slow is optimal, and optimal is expensive 
Biology Letters  2014;10(1):20131006.
When humans wish to move sideways, they almost never walk sideways, except for a step or two; they usually turn and walk facing forward. Here, we show that the experimental metabolic cost of walking sideways, per unit distance, is over three times that of forward walking. We explain this high metabolic cost with a simple mathematical model; sideways walking is expensive because it involves repeated starting and stopping. When walking sideways, our subjects preferred a low natural speed, averaging 0.575 m s−1 (0.123 s.d.). Even with no prior practice, this preferred sideways walking speed is close to the metabolically optimal speed, averaging 0.610 m s−1 (0.064 s.d.). Subjects were within 2.4% of their optimal metabolic cost per distance. Thus, we argue that sideways walking is avoided because it is expensive and slow, and it is slow because the optimal speed is low, not because humans cannot move sideways fast.
PMCID: PMC3917343  PMID: 24429685
legged locomotion; walking; metabolic energy cost; optimality; minimization; mathematical model
13.  Ubx promotes corbicular development in Apis mellifera 
Biology Letters  2014;10(1):20131021.
The key morphological feature that distinguishes corbiculate bees from other members of the Apidae family is the presence of the corbicula (pollen basket) on the tibial segment of hind legs. Here, we show that in the honeybee (Apis mellifera), the depletion of the gene Ultrabithorax (Ubx) by RNAi transforms the corbicula from a smooth, bristle-free concave structure to one covered with bristles. This is accompanied by a reduction of the pollen press, which is located on the basitarsus and used for packing the pollen pellet as well as a loss of the orderly arrangement of the rows of bristles that form the pollen comb. All these changes make the overall identity of workers’ T3 legs assume that of the queen. Furthermore, in a corbiculate bee of a different genus, Bombus impatiens, Ubx expression is also localized in T3 tibia and basitarsus. These observations suggest that the evolution of the pollen gathering apparatus in corbiculate bees may have a shared origin and could be traced to the acquisition of novel functions by Ubx, which in Apis were instrumental for subsequent castes and behavioural differentiation.
PMCID: PMC3917345  PMID: 24478202
honeybee; pollen basket; Ubx
14.  Ejaculate economics: an experimental test in a moth 
Biology Letters  2014;10(1):20131031.
Increasing evidence shows that spermatogenesis is costly. As a consequence, males should optimize the use of their sperm to maximize their reproductive outputs in their lifetime. However, experimental evidence on this prediction is largely lacking. Here, we examine how a male moth Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) responds to the presence of rivals or additional mates and how such response influences his lifetime reproductive fitness. We show that when rival males are present around a copulating pair, the male ejaculates more sperm to win a sperm competition battle but in such an environment he inseminates fewer females, sires fewer offspring and lives shorter. The opposite is the case when additional females are present during copulation. These findings reveal that elevated reproductive expenditure owing to sperm competition intensity is made at the expense of longevity and future reproduction.
PMCID: PMC3917346  PMID: 24429687
Ephestia kuehniella; sperm allocation; sperm competition intensity; male lifetime reproductive fitness
15.  Trophic convergence drives morphological convergence in marine tetrapods 
Biology Letters  2015;11(1):20140709.
Marine tetrapod clades (e.g. seals, whales) independently adapted to marine life through the Mesozoic and Caenozoic, and provide iconic examples of convergent evolution. Apparent morphological convergence is often explained as the result of adaptation to similar ecological niches. However, quantitative tests of this hypothesis are uncommon. We use dietary data to classify the feeding ecology of extant marine tetrapods and identify patterns in skull and tooth morphology that discriminate trophic groups across clades. Mapping these patterns onto phylogeny reveals coordinated evolutionary shifts in diet and morphology in different marine tetrapod lineages. Similarities in morphology between species with similar diets—even across large phylogenetic distances—are consistent with previous hypotheses that shared functional constraints drive convergent evolution in marine tetrapods.
PMCID: PMC4321144  PMID: 25631228
marine mammal; marine reptile; convergent evolution; feeding adaptation; functional morphology
16.  The cost of migration: spoonbills suffer higher mortality during trans-Saharan spring migrations only 
Biology Letters  2015;11(1):20140944.
Explanations for the wide variety of seasonal migration patterns of animals all carry the assumption that migration is costly and that this cost increases with migration distance. Although in some studies, the relationships between migration distance and breeding success or annual survival are established, none has investigated whether mortality during the actual migration increases with migration distance. Here, we compared seasonal survival between Eurasian spoonbills (Platalea leucorodia leucorodia) that breed in The Netherlands and migrate different distances (ca 1000, 2000 and 4500 km) to winter in France, Iberia and Mauritania, respectively. On the basis of resightings of individually marked birds throughout the year between 2005 and 2012, we show that summer, autumn and winter survival were very high and independent of migration distance, whereas mortality during spring migration was much higher (18%) for the birds that wintered in Mauritania, compared with those flying only as far as France (5%) or Iberia (6%). As such, this study is the first to show empirical evidence for increased mortality during some long migrations, likely driven by the presence of a physical barrier (the Sahara desert) in combination with suboptimal fuelling and unfavourable weather conditions en route.
PMCID: PMC4321157  PMID: 25589489
seasonal survival; mark–recapture analysis; differential migration; evolution of migration; long-distance migration; Sahara desert
17.  Bearded ladies: females suffer fitness consequences when bearing male traits 
Biology Letters  2013;9(6):20130644.
A central assumption in evolutionary biology is that females of sexually dimorphic species suffer costs when bearing male secondary sexual traits, such as ornamentation. Nevertheless, it is common in nature to observe females bearing rudimentary versions of male ornaments (e.g. ‘bearded ladies’), as ornaments can be under similar genetic control in both sexes. Here, we provide evidence that masculinized females incur both social and reproductive costs in nature. Male fence lizards (Sceloporus undulatus) discriminated against ornamented females during mate choice. Ornamented females had lower reproductive output, and produced eggs that were laid and hatched later than those of non-ornamented females. These findings support established theories of the evolution of sexual dimorphism and intralocus sexual conflict, and raise questions regarding the persistence of masculinizing ornamentation in females.
PMCID: PMC3871349  PMID: 24196514
intralocus sexual conflict; mate choice; Sceloporus undulatus; sexual dimorphism
18.  Imprinted green beards: a little less than kin and more than kind 
Biology Letters  2013;9(6):20130199.
RNA is complementary to the DNA sequence from which it is transcribed. Therefore, interactions between DNA and RNA provide a simple mechanism of genetic self-detection within nuclei. Imprinted RNAs could enable alleles of maternal and paternal origin to detect whether they are the same (homozygous) or different (heterozygous), and thereby provide strategic information about expected relatedness to siblings.
PMCID: PMC3871330  PMID: 24132086
inclusive fitness; imprinting; siRNA; green beards; relatedness
19.  Kin selection, genomics and caste-antagonistic pleiotropy 
Biology Letters  2013;9(6):20130309.
Kin selection is a fundamentally important process that affects the evolution of social behaviours. The genomics revolution now provides the opportunity to test kin selection theory using genomic data. In this commentary, we discuss previous studies that explored the link between kin selection and patterns of variation within the genome. We then present a new theory aimed at understanding the evolution of genes involved in the development of social insects. Specifically, we investigate caste-antagonistic pleiotropy, which occurs when the phenotypes of distinct castes are optimized by different genotypes at a single locus. We find that caste-antagonistic pleiotropy leads to narrow regions where polymorphism can be maintained. Furthermore, multiple mating by queens reduces the region in which worker-favoured alleles fix, which suggests that multiple mating impedes worker caste evolution. We conclude by discussing ways to test these and other facets of kin selection using newly emerging genomic data.
PMCID: PMC3871331  PMID: 24132087
antagonistic selection; eusocial insect caste; molecular evolution; sexual selection; social conflict
20.  Towards greater realism in inclusive fitness models: the case of worker reproduction in insect societies 
Biology Letters  2013;9(6):20130334.
The conflicts over sex allocation and male production in insect societies have long served as an important test bed for Hamilton's theory of inclusive fitness, but have for the most part been considered separately. Here, we develop new coevolutionary models to examine the interaction between these two conflicts and demonstrate that sex ratio and colony productivity costs of worker reproduction can lead to vastly different outcomes even in species that show no variation in their relatedness structure. Empirical data on worker-produced males in eight species of Melipona bees support the predictions from a model that takes into account the demographic details of colony growth and reproduction. Overall, these models contribute significantly to explaining behavioural variation that previous theories could not account for.
PMCID: PMC3871332  PMID: 24132088
social insects; worker reproduction; worker policing; sex allocation; inclusive fitness
21.  Hamiltonian inclusive fitness: a fitter fitness concept 
Biology Letters  2013;9(6):20130335.
In 1963–1964 W. D. Hamilton introduced the concept of inclusive fitness, the only significant elaboration of Darwinian fitness since the nineteenth century. I discuss the origin of the modern fitness concept, providing context for Hamilton's discovery of inclusive fitness in relation to the puzzle of altruism. While fitness conceptually originates with Darwin, the term itself stems from Spencer and crystallized quantitatively in the early twentieth century. Hamiltonian inclusive fitness, with Price's reformulation, provided the solution to Darwin's ‘special difficulty’—the evolution of caste polymorphism and sterility in social insects. Hamilton further explored the roles of inclusive fitness and reciprocation to tackle Darwin's other difficulty, the evolution of human altruism. The heuristically powerful inclusive fitness concept ramified over the past 50 years: the number and diversity of ‘offspring ideas’ that it has engendered render it a fitter fitness concept, one that Darwin would have appreciated.
PMCID: PMC3871333  PMID: 24132089
Darwinian fitness; inclusive fitness; Hamilton's rule; kin selection; social evolution; altruism
22.  The veil of ignorance can favour biological cooperation 
Biology Letters  2013;9(6):20130365.
Lack of information is a constraint but ignorance can sometimes assist the evolution of cooperation by constraining selfishness. We discuss examples involving both ignorance of role or pay-off and ignorance of relatedness. Ignorance can favour cooperative traits like grouping and warning coloration and reduce conflicts from meiotic drive, imprinting, greenbeards and various forms of nepotism.
PMCID: PMC3871334  PMID: 24132090
veil of ignorance; cooperation; conflict; relatedness; meiosis; nepotism
23.  Parasites and altruism: converging roads 
Biology Letters  2013;9(6):20130367.
W.D. Hamilton was most known for his work on two topics: social evolution and parasites. Although at first glance these seem to be disparate interests, they share many attributes and have logical connections within evolutionary biology. Nevertheless, Hamilton's contributions in these areas met with very different receptions, with his place in the field of social evolution assured, but his work on the role of parasites perceived as more specialized. We take an historical approach to examine the reasons for this difference.
PMCID: PMC3871335  PMID: 24132091
Hamilton; parasites; social evolution
24.  Genes underlying altruism 
Biology Letters  2013;9(6):20130395.
William D. Hamilton postulated the existence of ‘genes underlying altruism’, under the rubric of inclusive fitness theory, a half-century ago. Such genes are now poised for discovery. In this article, we develop a set of intuitive criteria for the recognition and analysis of genes for altruism and describe the first candidate genes affecting altruism from social insects and humans. We also provide evidence from a human population for genetically based trade-offs, underlain by oxytocin-system polymorphisms, between alleles for altruism and alleles for non-social cognition. Such trade-offs between self-oriented and altruistic behaviour may influence the evolution of phenotypic diversity across all social animals.
PMCID: PMC3871336  PMID: 24132092
altruism; inclusive fitness; sociality
25.  The drivers of woody species richness and density in a Neotropical savannah 
Biology Letters  2013;9(6):20130412.
Environmental filtering prevents species without certain attributes from occurring in local communities. Traits respond differently to different abiotic factors, assembling communities with varying composition along environmental gradients. Here, we measured proxies of soil fertility, disturbance by fire, response and physiological traits to assess how these variables interact to determine woody species richness and density in a Neotropical savannah. We explicitly incorporated our assumptions about how different abiotic filters influence different subsets of traits into a statistical model using structural equation modelling, yielding a more accurate representation of the assembly process. Fire had an effect on resistance traits, whereas soil fertility influenced physiological traits. Resistance traits explained both the richness and density of plots, whereas physiological traits explained only the density. Fewer fire events led to richer and denser plots. Similarly, areas with lower cation exchange capacity assembled less dense communities. Furthermore, we showed that structural equation modelling yielded a realistic representation of the bivariate interactions of distinct environmental filters with different subsets of traits.
PMCID: PMC3871337  PMID: 24152692
cerrado; community assembly; savannah; structural equation modelling; traits

Results 1-25 (2090)