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26.  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
27.  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
28.  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
29.  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
30.  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
31.  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
32.  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
33.  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
34.  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
35.  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
36.  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
37.  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
38.  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
39.  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
40.  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
41.  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
42.  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
43.  Dissecting ant recognition systems in the age of genomics 
Biology Letters  2013;9(6):20130416.
Hamilton is probably best known for his seminal work demonstrating the role of kin selection in social evolution. His work made it clear that, for individuals to direct their altruistic behaviours towards appropriate recipients (kin), mechanisms must exist for kin recognition. In the social insects, colonies are typically comprised of kin, and colony recognition cues are used as proxies for kinship cues. Recent years have brought rapid advances in our understanding of the genetic and molecular mechanisms that are used for this process. Here, I review some of the most notable advances, particularly the contributions from recent ant genome sequences and molecular biology.
PMCID: PMC3871338  PMID: 24132093
Formicidae; genomics; chemosensory receptors; cuticular hydrocarbons
44.  Nice to kin and nasty to non-kin: revisiting Hamilton's early insights on eusociality 
Biology Letters  2013;9(6):20130444.
When helping behaviour is costly, Hamiltonian logic implies that animals need to direct helpful acts towards kin, so that indirect fitness benefits justify the costs. We revisit inferences about nepotism and aggression in Hamilton's 1964 paper to argue that he overestimated the general significance of nepotism, but that other issues that he raised continue to suggest novel research agendas today. We now know that nepotism in eusocial insects is rare, because variation in genetic recognition cues is insufficient. A lower proportion of individuals breeding and larger clutch sizes selecting for a more uniform colony odour may explain this. Irreversible worker sterility can induce both the fiercest possible aggression and the highest likelihood of helping random distant kin, but these Hamiltonian contentions still await large-scale testing in social animals.
PMCID: PMC3871339  PMID: 24132094
clutch size; recognition; Gestalt; inclusive fitness; nepotism; unmatedness
45.  Kinship and the evolution of social behaviours in the sea 
Biology Letters  2013;9(6):20130454.
Until recently, little attention has been paid to the existence of kin structure in the sea, despite the fact that many marine organisms are sessile or sedentary. This lack of attention to kin structure, and its impacts on social evolution, historically stems from the pervasive assumption that the dispersal of gametes and larvae is almost always sufficient to prevent any persistent associations of closely related offspring or adults. However, growing evidence, both theoretical and empirical, casts doubt on the generality of this assumption, not only in species with limited dispersal, but also in species with long dispersive phases. Moreover, many marine organisms either internally brood their progeny or package them in nurseries, both of which provide ample opportunities for kinship to influence the nature and outcomes of social interactions among family members. As the evidence for kin structure within marine populations mounts, it follows that kin selection may play a far greater role in the evolution of both behaviours and life histories of marine organisms than is presently appreciated.
PMCID: PMC3871340  PMID: 24132095
kin structure; social behaviour; cooperation; marine organisms; relatedness
46.  Kin selection, species richness and community 
Biology Letters  2013;9(6):20130491.
Can evolutionary and ecological dynamics operating at one level of the biological hierarchy affect the dynamics and structure at other levels? In social insects, strong hostility towards unrelated individuals can evolve as a kin-selected counter-adaptation to intraspecific social parasitism. This aggression in turn might cause intraspecific competition to predominate over interspecific competition, permitting coexistence with other social insect species. In other words, kin selection—a form of intra-population dynamics—might enhance the species richness of the community, a higher-level structure. The converse effect, from higher to lower levels, might also operate, whereby strong interspecific competition may limit the evolution of selfish individual traits. If the latter effect were to prove more important, it would challenge the common view that intra-population dynamics (via individual or gene selection) is the main driver of evolution.
PMCID: PMC3871341  PMID: 24132096
intra-population dynamics; evolution; competition; biological hierarchy
47.  Disruptive camouflage impairs object recognition 
Biology Letters  2013;9(6):20130501.
Whether hiding from predators, or avoiding battlefield casualties, camouflage is widely employed to prevent detection. Disruptive coloration is a seemingly well-known camouflage mechanism proposed to function by breaking up an object's salient features (for example their characteristic outline), rendering objects more difficult to recognize. However, while a wide range of animals are thought to evade detection using disruptive patterns, there is no direct experimental evidence that disruptive coloration impairs recognition. Using humans searching for computer-generated moth targets, we demonstrate that the number of edge-intersecting patches on a target reduces the likelihood of it being detected, even at the expense of reduced background matching. Crucially, eye-tracking data show that targets with more edge-intersecting patches were looked at for longer periods prior to attack, and passed-over more frequently during search tasks. We therefore show directly that edge patches enhance survivorship by impairing recognition, confirming that disruptive coloration is a distinct camouflage strategy, not simply an artefact of background matching.
PMCID: PMC3871342  PMID: 24152693
crypsis; background matching; disruptive coloration; vision; eye tracking; edge detection
48.  Social foragers adopt a riskier foraging mode in the centre of their groups 
Biology Letters  2013;9(6):20130528.
Foraging in groups provides many benefits that are not necessarily experienced the same way by all individuals. I explore the possibility that foraging mode, the way individuals exploit resources, varies as a function of spatial position in the group, reflecting commonly occurring spatial differences in predation risk. I show that semipalmated sandpipers (Calidris pusilla), a social foraging avian species, tended to adopt a riskier foraging mode in the central, more protected areas of their groups. Central birds effectively used the more peripheral group members as sentinels, allowing them to exploit a wider range of resources within the same group at the same time. This finding provides a novel benefit of living in groups, which may have a broad relevance given that social foraging species often exploit a large array of resources.
PMCID: PMC3871343  PMID: 24108674
antipredator vigilance; semipalmated sandpipers; social foraging; spatial position
49.  Immune-priming in ant larvae: social immunity does not undermine individual immunity 
Biology Letters  2013;9(6):20130563.
Social insects deploy numerous strategies against pathogens including behavioural, biochemical and immunological responses. While past research has revealed that adult social insects can generate immunity, few studies have focused on the immune function during an insect's early life stages. We hypothesized that larvae of the black carpenter ant Camponotus pennsylvanicus vaccinated with heat-killed Serratia marcescens should be less susceptible to a challenge with an active and otherwise lethal dose of the bacterium. We compared the in vivo benefits of prior vaccination of young larvae relative to naive and ringer injected controls. Regardless of colony of origin, survival parameters of vaccinated individuals following a challenge were significantly higher than those of the other two treatments. Results support the hypothesis that ant larvae exhibit immune-priming. Based on these results, we can infer that brood care by workers does not eliminate the need for individual-level immunological responses. Focusing on these early stages of development within social insect colonies can start addressing the complex dynamics between physiological (individual level) and social (collective) immunity.
PMCID: PMC3871344  PMID: 24108675
social insects; Camponotus pennsylvanicus; individual versus social immunity
50.  The early bird gets the worm: foraging strategies of wild songbirds lead to the early discovery of food sources 
Biology Letters  2013;9(6):20130578.
Animals need to manage the combined risks of predation and starvation in order to survive. Theoretical and empirical studies have shown that individuals can reduce predation risk by delaying feeding (and hence fat storage) until late afternoon. However, little is known about how individuals manage the opposing pressures of resource uncertainty and predation risks. We suggest that individuals should follow a two-part strategy: prioritizing the discovery of food early in the day and exploiting the best patch late in the day. Using automated data loggers, we tested whether a temporal component exists in the discovery of novel foraging locations by individuals in a mixed-species foraging guild. We found that food deployed in the morning was discovered significantly more often than food deployed in the afternoon. Based on the diurnal activity patterns in this population, overall rates of new arrivals were also significantly higher than expected in the morning and significantly lower than expected in the afternoon. These results align with our predictions of a shift from patch discovery to exploitation over the course of the day.
PMCID: PMC3871345  PMID: 24108676
predation; starvation; foraging strategies; food hoarding

Results 26-50 (2110)