Recently, the debate on the origins of the major European Y chromosome haplogroup R1b1b2-M269 has reignited, and opinion has moved away from Palaeolithic origins to the notion of a younger Neolithic spread of these chromosomes from the Near East. Here, we address this debate by investigating frequency patterns and diversity in the largest collection of R1b1b2-M269 chromosomes yet assembled. Our analysis reveals no geographical trends in diversity, in contradiction to expectation under the Neolithic hypothesis, and suggests an alternative explanation for the apparent cline in diversity recently described. We further investigate the young, STR-based time to the most recent common ancestor estimates proposed so far for R-M269-related lineages and find evidence for an appreciable effect of microsatellite choice on age estimates. As a consequence, the existing data and tools are insufficient to make credible estimates for the age of this haplogroup, and conclusions about the timing of its origin and dispersal should be viewed with a large degree of caution.
Y-STRs; R1b1b2-M269; neolithic hypothesis; average squared distance
Though Pleistocene refugia are frequently cited as drivers of species diversification, comparisons of molecular divergence among sister species typically indicate a continuum of divergence times from the Late Miocene, rather than a clear pulse of speciation events at the Last Glacial Maximum. Community-scale inference methods that explicitly test for multiple vicariance events, and account for differences in ancestral effective population size and gene flow, are well suited for detecting heterogeneity of species' responses to past climate fluctuations. We apply this approach to multi-locus sequence data from five co-distributed frog species endemic to the Wet Tropics rainforests of northeast Australia. Our results demonstrate at least two episodes of vicariance owing to climate-driven forest contractions: one in the Early Pleistocene and the other considerably older. Understanding how repeated cycles of rainforest contraction and expansion differentially affected lineage divergence among co-distributed species provides a framework for identifying evolutionary processes that underlie population divergence and speciation.
community phylogeography; lineage divergence; Litoria; Australia Wet Tropics
While biochemical mechanisms are typically used by animals to reduce oxidative damage, insects are suspected to employ a higher organizational level, discontinuous gas exchange mechanism to do so. Using a combination of real-time, flow-through respirometry and live-cell fluorescence microscopy, we show that spiracular control associated with the discontinuous gas exchange cycle (DGC) in Samia cynthia pupae is related to reactive oxygen species (ROS). Hyperoxia fails to increase mean ROS production, although minima are elevated above normoxic levels. Furthermore, a negative relationship between mean and mean ROS production indicates that higher ROS production is generally associated with lower . Our results, therefore, suggest a possible signalling role for ROS in DGC, rather than supporting the idea that DGC acts to reduce oxidative damage by regulating ROS production.
discontinuous gas exchange; periodic ventilation; adaptation; metabolism; oxidative damage; trachea
Plant nuclear genome size (GS) varies over three orders of magnitude and is correlated with cell size and growth rate. We explore whether these relationships can be owing to geometrical scaling constraints. These would produce an isometric GS–cell volume relationship, with the GS–cell diameter relationship with the exponent of 1/3. In the GS–cell division relationship, duration of processes limited by membrane transport would scale at the 1/3 exponent, whereas those limited by metabolism would show no relationship. We tested these predictions by estimating scaling exponents from 11 published datasets on differentiated and meristematic cells in diploid herbaceous plants. We found scaling of GS–cell size to almost perfectly match the prediction. The scaling exponent of the relationship between GS and cell cycle duration did not match the prediction. However, this relationship consists of two components: (i) S phase duration, which depends on GS, and has the predicted 1/3 exponent, and (ii) a GS-independent threshold reflecting the duration of the G1 and G2 phases. The matches we found for the relationships between GS and both cell size and S phase duration are signatures of geometrical scaling. We propose that a similar approach can be used to examine GS effects at tissue and whole plant levels.
scaling exponent; standard major axis regression regression; nuclear size; cell size; cell cycle phases; root meristem
Herbivores have been hypothesized to adapt locally to variation in plant defences and such adaptation could facilitate novel associations in the context of biological invasions. Here, we show that in the native range of the viburnum leaf beetle (VLB, Pyrrhalta viburni), two populations of geographically isolated hosts—Viburnum opulus and Viburnum tinus—have divergent defences against VLB oviposition: negative versus positive density-dependent egg-crushing wound responses, respectively. Populations of beetles coexisting with each host show an adaptive behavioural response: aggregative versus non-aggregative oviposition on V. opulus and V. tinus, respectively. In parallel, we show that in North America, where VLB is invasive, defences of three novel hosts are negatively density-dependent, and beetles' oviposition behaviour is aggregative. Thus, local adaptation to plant defences has the potential to facilitate the invasion of herbivores onto novel hosts.
insect oviposition strategy; invasion ecology; adaptive deme hypothesis; Chrysomelidae; plant–insect interactions; plant defence theory
Recent studies have demonstrated a role for the elastic protein titin in active muscle, but the mechanisms by which titin plays this role remain to be elucidated. In active muscle, Ca2+-binding has been shown to increase titin stiffness, but the observed increase is too small to explain the increased stiffness of parallel elastic elements upon muscle activation. We propose a ‘winding filament’ mechanism for titin's role in active muscle. First, we hypothesize that Ca2+-dependent binding of titin's N2A region to thin filaments increases titin stiffness by preventing low-force straightening of proximal immunoglobulin domains that occurs during passive stretch. This mechanism explains the difference in length dependence of force between skeletal myofibrils and cardiac myocytes. Second, we hypothesize that cross-bridges serve not only as motors that pull thin filaments towards the M-line, but also as rotors that wind titin on the thin filaments, storing elastic potential energy in PEVK during force development and active stretch. Energy stored during force development can be recovered during active shortening. The winding filament hypothesis accounts for force enhancement during stretch and force depression during shortening, and provides testable predictions that will encourage new directions for research on mechanisms of muscle contraction.
connectin; force enhancement; force depression; history dependence of force production; thin filament rotation; titin–actin interactions
The small size of the billions of migrating songbirds commuting between temperate breeding sites and the tropics has long prevented the study of the largest part of their annual cycle outside the breeding grounds. Using light-level loggers (geolocators), we recorded the entire annual migratory cycle of the red-backed shrike Lanius collurio, a trans-equatorial Eurasian-African passerine migrant. We tested differences between autumn and spring migration for nine individuals. Duration of migration between breeding and winter sites was significantly longer in autumn (average 96 days) when compared with spring (63 days). This difference was explained by much longer staging periods during autumn (71 days) than spring (9 days). Between staging periods, the birds travelled faster during autumn (356 km d–1) than during spring (233 km d–1). All birds made a protracted stop (53 days) in Sahelian sub-Sahara on southbound migration. The birds performed a distinct loop migration (22 000 km) where spring distance, including a detour across the Arabian Peninsula, exceeded the autumn distance by 22 per cent. Geographical scatter between routes was particularly narrow in spring, with navigational convergence towards the crossing point from Africa to the Arabian Peninsula. Temporal variation between individuals was relatively constant, while different individuals tended to be consistently early or late at different departure/arrival occasions during the annual cycle. These results demonstrate the existence of fundamentally different spatio-temporal migration strategies used by the birds during autumn and spring migration, and that songbirds may rely on distinct staging areas for completion of their annual cycle, suggesting more sophisticated endogenous control mechanisms than merely clock-and-compass guidance among terrestrial solitary migrants. After a century with metal-ringing, year-round tracking of long-distance migratory songbirds promises further insights into bird migration.
avian migration; geolocator; passerine; migration speed; phenology; migration routes
Despite observational evidence of carry-over effects (COEs, events occurring in one season that produce residual effects on individuals the following seasons), to our knowledge no experimental studies have been carried out to explore how COEs might affect reproductive output. We simulated an environmental perturbation affecting spring-staging migrants to investigate COEs in greater snow geese (Anser caerulescens atlanticus). During three consecutive years, 2037 females captured during spring staging (approx. 3000 km south of their Arctic breeding grounds) were maintained in captivity (with or without access to food) for 0–4 days. Duration of captivity (but not food treatment) negatively affected reproductive success, probably through stress response. Reproductive success was reduced by 45–71% in 2 years, but not in a third year with unusually favourable breeding conditions. This unprecedented manipulation indicates that COEs can have a strong effect on individual reproductive success in long-distance migrants, but that this effect can be partly compensated for by good environmental conditions on the breeding ground.
bird migration; carry-over effects; compensation; snow geese
Many vertebrates eavesdrop on alarm calls of other species, which is a remarkable ability, given geographical variation in community composition and call diversity within and among species. We used micro-geographical variation in community composition to test whether individuals recognize heterospecific alarm calls by: (i) responding to acoustic features shared among alarm calls; (ii) having innate responses to particular heterospecific calls; or (iii) learning specific alarm calls. We found that superb fairy-wrens (Malurus cyaneus) fled to cover to playback of noisy miner (Manorina melanocephala) aerial predator alarm calls only in locations where miners were present, suggesting that learning rather than acoustic structure determines response. Sites with and without miners were well within the dispersal distance of fairy-wrens, and philopatric males and dispersing females showed the same pattern, so that local genetic adaptation is extremely unlikely. Furthermore, where miners were present, fairy-wrens responded appropriately to different miner calls, implying eavesdropping on their signalling system rather than fleeing from miners themselves. Learned eavesdropping on alarm calls enables individuals to harvest ecologically relevant information from heterospecifics on an astonishingly fine spatial scale. Such phenotypic plasticity is valuable in a changing world, where individuals can be exposed to new species.
interspecific communication; eavesdropping; alarm calls; acoustic communication; learning
Giant suspension feeders such as mysticete whales, basking and whale sharks, and the extinct (indicated by ‘†’) †pachycormiform teleosts are conspicuous members of modern and fossil marine vertebrate faunas. Whether convergent anatomical features common to these clades arose along similar evolutionary pathways has remained unclear because of a lack of information surrounding the origins of all groups of large-bodied suspension feeders apart from baleen whales. New investigation reveals that the enigmatic ray-finned fish †Ohmdenia, from the Lower Jurassic (Toarcian, 183.0–175.6 Ma) Posidonia Shale Lagerstätte, represents the immediate sister group of edentulous †pachycormiforms, the longest lived radiation of large vertebrate suspension feeders. †Ohmdenia bisects the long morphological branch leading to suspension-feeding †pachycormiforms, providing information on the sequence of anatomical transformations preceding this major ecological shift that can be compared to changes associated with the origin of modern mysticetes. Similarities include initial modifications to jaw geometry associated with the reduction of dentition, followed by the loss of teeth. The evolution of largest body sizes within both radiations occurs only after the apparent onset of microphagy. Comparing the fit of contrasting evolutionary models to functionally relevant morphological measurements for whales and †pachycormiform fishes reveals strong support for a common adaptive peak shared by suspension-feeding members of both clades.
Cetacea; convergent evolution; filter feeding; Mysticeti; planktivory; stem teleost
Bilateral symmetry is visually salient to diverse animals including birds, but whereas experimental studies typically use bilaterally symmetrical two-dimensional patterns that are viewed approximately fronto-parallel; in nature, animals observe three-dimensional objects from all angles. Many animals and plant structures have a plane of bilateral symmetry. Here, we first (experiment I) give evidence that young poultry chicks readily generalize bilateral symmetry as a feature of two-dimensional patterns in fronto-parallel view. We then test the ability of chicks to recognize symmetry in images that would be produced by the transformed view produced by a 40° horizontal combined with a 20° vertical rotation of a pattern on a spherical surface. Experiment II gives evidence that chicks trained to distinguish symmetrical from asymmetrical patterns treat rotated views of symmetrical ‘objects’ as symmetrical. Experiment III gives evidence that chicks trained to discriminate rotated views of symmetrical ‘objects’ from asymmetrical patterns generalize to novel symmetrical objects either in fronto-parallel or rotated view. These findings emphasize the importance of bilateral symmetry for three-dimensional object recognition and raise questions about the underlying mechanisms of symmetry perception.
symmetry; vision; object recognition; domestic chick; categorization
Lithodid crabs (and other skeleton-crushing predators) may have been excluded from cold Antarctic continental shelf waters for more than 14 Myr. The west Antarctic Peninsula shelf is warming rapidly and has been hypothesized to be soon invaded by lithodids. A remotely operated vehicle survey in Palmer Deep, a basin 120 km onto the Antarctic shelf, revealed a large, reproductive population of lithodids, providing the first evidence that king crabs have crossed the Antarctic shelf. DNA sequencing and morphology indicate the lithodid is Neolithodes yaldwyni Ahyong & Dawson, previously reported only from Ross Sea waters. We estimate a N. yaldwyni population density of 10 600 km−2 and a population size of 1.55 × 106 in Palmer Deep, a density similar to lithodid populations of commercial interest around Alaska and South Georgia. The lithodid occurred at depths of more than 850 m and temperatures of more than 1.4°C in Palmer Deep, and was not found in extensive surveys of the colder shelf at depths of 430–725 m. Where N. yaldwyni occurred, crab traces were abundant, megafaunal diversity reduced and echinoderms absent, suggesting that the crabs have major ecological impacts. Antarctic Peninsula shelf waters are warming at approximately 0.01°C yr−1; if N. yaldwyni is currently limited by cold temperatures, it could spread up onto the shelf (400–600 m depths) within 1–2 decades. The Palmer Deep N. yaldwyni population provides an important model for the potential invasive impacts of crushing predators on vulnerable Antarctic shelf ecosystems.
lithodids; invasion; Antarctic; climate warming; bioturbation; biodiversity loss
How do biogeographically different provinces arise in response to oceanic barriers to dispersal? Here, we analyse how traits related to the pelagic dispersal and adult biology of 985 tropical reef fish species correlate with their establishing populations on both sides of two Atlantic marine barriers: the Mid-Atlantic Barrier (MAB) and the Amazon–Orinoco Plume (AOP). Generalized linear mixed-effects models indicate that predictors for successful barrier crossing are the ability to raft with flotsam for the deep-water MAB, non-reef habitat usage for the freshwater and sediment-rich AOP, and large adult-size and large latitudinal-range for both barriers. Variation in larval-development mode, often thought to be broadly related to larval-dispersal potential, is not a significant predictor in either case. Many more species of greater taxonomic diversity cross the AOP than the MAB. Rafters readily cross both barriers but represent a much smaller proportion of AOP crossers than MAB crossers. Successful establishment after crossing both barriers may be facilitated by broad environmental tolerance associated with large body size and wide latitudinal-range. These results highlight the need to look beyond larval-dispersal potential and assess adult-biology traits when assessing determinants of successful movements across marine barriers.
macroecology; biogeographic barriers; Amazon–Orinoco Plume; rafting; larval-development mode; body size
Variation in the physical characteristics of the environment should impact the movement energetics of animals. Although cognizance of this may help interpret movement ecology, determination of the landscape-dependent energy expenditure of wild animals is problematic. We used accelerometers in animal-attached tags to derive energy expenditure in 54 free-living imperial cormorants Phalacrocorax atriceps and construct an energy landscape of the area around a breeding colony. Examination of the space use of a further 74 birds over 4 years showed that foraging areas selected varied considerably in distance from the colony and water depth, but were characterized by minimal power requirements compared with other areas in the available landscape. This accords with classic optimal foraging concepts, which state that animals should maximize net energy gain by minimizing costs where possible and show how deriving energy landscapes can help understand how and why animals distribute themselves in space.
energy landscape; movement ecology; metabolic power; area use; foraging efficiency
In many species, each female pairs with a single male for the purpose of rearing offspring, but may also engage in extra-pair copulations. Despite the prevalence of such promiscuity, whether and how multiple mating benefits females remains an open question. Multiple mating is typically thought to be favoured primarily through indirect benefits (i.e. heritable effects on the fitness of offspring). This prediction has been repeatedly tested in a variety of species, but the evidence has been equivocal, perhaps because such studies have focused on pre-reproductive survival rather than lifetime fitness of offspring. Here, we show that in a songbird, the dark-eyed junco (Junco hyemalis), both male and female offspring produced by extra-pair fertilizations have higher lifetime reproductive success than do offspring sired within the social pair. Furthermore, adult male offspring sired via extra-pair matings are more likely to sire extra-pair offspring (EPO) themselves, suggesting that fitness benefits to males accrue primarily through enhanced mating success. By contrast, female EPO benefited primarily through enhanced fecundity. Our results provide strong support for the hypothesis that the evolution of extra-pair mating by females is favoured by indirect benefits and shows that such benefits accrue much later in the offspring's life than previously documented.
extra-pair mating; multiple mating; lifetime reproductive success; indirect fitness benefits; sexual selection
How and why diverse sexual systems evolve are fascinating evolutionary questions, but few empirical studies have dealt with these questions in animals. Pedunculate (gooseneck) barnacles show such diversity, including simultaneous hermaphroditism, coexistence of dwarf males and hermaphrodites (androdioecy), and coexistence of dwarf males and females (dioecy). Here, we report the first phylogenetically controlled test of the hypothesis that the ultimate cause of the diverse sexual systems and presence of dwarf males in this group is limited mating opportunities for non-dwarf individuals, owing to mating in small groups. Within the pedunculate barnacle phylogeny, dwarf males and females have evolved repeatedly. Females are more likely to evolve in androdioecious than hermaphroditic populations, suggesting that evolution of dwarf males has preceded that of females in pedunculates. Both dwarf males and females are associated with a higher proportion of solitary individuals in the population, corroborating the hypothesis that limited mating opportunities have favoured evolution of these diverse sexual systems, which have puzzled biologists since Darwin.
androdioecy; dwarf male; mating system; phylogeny; sexuality pattern
Eggs are an immobile, vulnerable stage of development and their success often depends on the oviposition decisions of the mother. Studies show that female animals, and sometimes males, may invest parental resources in order to increase the survival of their offspring. Here, we describe a unique form of parental investment in offspring survival. The seed beetle Mimosestes amicus may lay eggs singly, or may cover eggs with additional egg(s). This egg stacking serves to significantly reduce the mortality of the protected egg from parasitism by the parasitic wasp, Uscana semifumipennis. The smaller top eggs serve only as protective shields; they are inviable, and wasps that develop in them suffer negative fitness consequences. Further, we found egg stacking to be inducible; M. amicus increase the number of stacks they lay when parasitoids are present. However, stacking invokes a cost. When wasps are absent, beetles lay more single eggs, and produce more offspring, highlighting the adaptive value of this extraordinary example of behavioural plasticity in parental investment.
egg stacking; offspring quality versus quantity; life-history trade-offs; seed beetles; Mimosestes amicus; offspring defence
Africa hosts a single breeding species of penguin today, yet the fossil record indicates that a diverse array of now-extinct taxa once inhabited southern African coastlines. Here, we show that the African penguin fauna had a complex history involving multiple dispersals and extinctions. Phylogenetic analyses and biogeographic reconstructions incorporating new fossil material indicate that, contrary to previous hypotheses, the four Early Pliocene African penguin species do not represent an endemic radiation or direct ancestors of the living Spheniscus demersus (blackfooted penguin). A minimum of three dispersals to Africa, probably assisted by the eastward-flowing Antarctic Circumpolar and South Atlantic currents, occurred during the Late Cenozoic. As regional sea-level fall eliminated islands and reduced offshore breeding areas during the Pliocene, all but one penguin lineage ended in extinction, resulting in today's depleted fauna.
biogeography; South Atlantic Gyre; fossil; Pliocene; phylogeny
Reliable estimates of time are essential for initiating interceptive actions at the right moment. However, our sense of time is surprisingly fallible. For instance, time perception can be distorted by prolonged exposure (adaptation) to movement. Here, we make use of this to determine if time perception and anticipatory actions rely on the same or on different temporal metrics. Consistent with previous reports, we find that the apparent duration of movement is mitigated by adaptation to more rapid motion, but is unchanged by adaptation to slower movement. By contrast, we find symmetrical effects of motion-adaptation on the timing of anticipatory interceptive actions, which are paralleled by changes in perceived speed for the adapted direction of motion. Our data thus reveal that anticipatory actions and perceived duration rely on different temporal metrics.
action; interception; perception; time perception
To study the function of pearl oyster matrix proteins in nacreous layer biomineralization in vivo, we examined the deposition on pearl nuclei and the expression of matrix protein genes in the pearl sac during the early stage of pearl formation. We found that the process of pearl formation involves two consecutive stages: (i) irregular calcium carbonate (CaCO3) deposition on the bare nucleus and (ii) CaCO3 deposition that becomes more and more regular until the mature nacreous layer has formed on the nucleus. The low-expression level of matrix proteins in the pearl sac during periods of irregular CaCO3 deposition suggests that deposition may not be controlled by the organic matrix during this stage of the process. However, significant expression of matrix proteins in the pearl sac was detected by day 30–35 after implantation. On day 30, a thin layer of CaCO3, which we believe was amorphous CaCO3, covered large aragonites. By day 35, the nacreous layer had formed. The whole process is similar to that observed in shells, and the temporal expression of matrix protein genes indicated that their bioactivities were crucial for pearl development. Matrix proteins controlled the crystal phase, shape, size, nucleation and aggregation of CaCO3 crystals.
pearl formation; Pinctada fucata; nacre matrix proteins; real-time PCR; gene expression
The study of animal cognition has provided valuable data throughout the years, yet its reliance on laboratory work leaves some open questions. The main question is whether animals employ cognition in daily decision-making. The following discussion uses sperm competition (SC) as a test case for demonstrating the effect of cognition on routine choices, in this case, sexual selection. Cognition is manifested here by males' ability to represent the number of rivals competing with them. I claim that response to SC is driven by quantity estimation and the ability to assess competition magnitude cognitively. Hence, cognition can determine males' response to SC, and consequentially it can be selected within this context. This supports the argument that cognition constitutes an integral part of an individual's toolbox in solving real-life problems, and shows that physical and behavioural phenomena can expose cognition to selection and facilitate its evolution.
animal cognition; sperm competition; quantity estimation; evolution; sexual selection; cognition
Marine protected areas (MPAs) are increasingly implemented as tools to conserve and manage fisheries and target species. Because there are opportunity costs to conservation, there is a need for science-based assessment of MPAs. Here, we present one of the northernmost documentations of MPA effects to date, demonstrated by a replicated before–after control-impact (BACI) approach. In 2006, MPAs were implemented along the Norwegian Skagerrak coast offering complete protection to shellfish and partial protection to fish. By 2010, European lobster (Homarus gammarus) catch-per-unit-effort (CPUE) had increased by 245 per cent in MPAs, whereas CPUE in control areas had increased by 87 per cent. Mean size of lobsters increased by 13 per cent in MPAs, whereas increase in control areas was negligible. Furthermore, MPA-responses and population development in control areas varied significantly among regions. This illustrates the importance of a replicated BACI design for reaching robust conclusions and management decisions. Partial protection of Atlantic cod (Gadus morhua) was followed by an increase in population density and body size compared with control areas. By 2010, MPA cod were on average 5 cm longer than in any of the control areas. MPAs can be useful management tools in rebuilding and conserving portions of depleted lobster populations in northern temperate waters, and even for a mobile temperate fish species such as the Atlantic cod.
before–after control-impact; marine reserves; baseline information; mark–recapture; Gadus morhua; Homarus gammarus
Gleaning insectivorous bats that forage by using echolocation within dense forest vegetation face the sensorial challenge of acoustic masking effects. Active perception of silent and motionless prey in acoustically cluttered environments by echolocation alone has thus been regarded impossible. The gleaning insectivorous bat Micronycteris microtis however, forages in dense understory vegetation and preys on insects, including dragonflies, which rest silent and motionless on vegetation. From behavioural experiments, we show that M. microtis uses echolocation as the sole sensorial modality for successful prey perception within a complex acoustic environment. All individuals performed a stereotypical three-dimensional hovering flight in front of prey items, while continuously emitting short, multi-harmonic, broadband echolocation calls. We observed a high precision in target localization which suggests that M. microtis perceives a detailed acoustic image of the prey based on shape, surface structure and material. Our experiments provide, to our knowledge, the first evidence that a gleaning bat uses echolocation alone for successful detection, classification and precise localization of silent and motionless prey in acoustic clutter. Overall, we conclude that the three-dimensional hovering flight of M. microtis in combination with a frequent emission of short, high-frequency echolocation calls is the key for active prey perception in acoustically highly cluttered environments.
prey perception; echolocation; acoustic clutter; narrow-space active gleaning insectivorous bat; Micronycteris microtis
Environmental problems have contributed to numerous collapses of civilizations in the past. Now, for the first time, a global collapse appears likely. Overpopulation, overconsumption by the rich and poor choices of technologies are major drivers; dramatic cultural change provides the main hope of averting calamity.
population; consumption; environment; agriculture; climate; culture