Genetic diversity within honeybee colonies increases signal production by waggle-dancing foragers

Recent work has demonstrated considerable benefits of intracolonial genetic diversity for the productivity of honeybee colonies: single-patriline colonies have depressed foraging rates, smaller food stores and slower weight gain relative to multiple-patriline colonies. We explored whether differences in the use of foraging-related communication behaviour (waggle dances and shaking signals) underlie differences in foraging effort of genetically diverse and genetically uniform colonies. We created three pairs of colonies; each pair had one colony headed by a multiply mated queen (inseminated by 15 drones) and one colony headed by a singly mated queen. For each pair, we monitored the production of foraging-related signals over the course of 3 days. Foragers in genetically diverse colonies had substantially more information available to them about food resources than foragers in uniform colonies. On average, in genetically diverse colonies compared with genetically uniform colonies, 36% more waggle dances were identified daily, dancers performed 62% more waggle runs per dance, foragers reported food discoveries that were farther from the nest and 91% more shaking signals were exchanged among workers each morning prior to foraging. Extreme polyandry by honeybee queens enhances the production of worker-worker communication signals that facilitate the swift discovery and exploitation of food resources.     

Larger trees may support larger Indiana bat maternity colonies in a dynamic landscape

Indiana bats (Myotis sodalis), federally listed as endangered, are of management concern in eastern North America. While researchers quantified the habitat affinities of the species throughout the range, few studies have occurred in regions where populations are at high risk for wind energy development and changing climes. Central Illinois, USA, is a dynamic landscape where forest area has been increasing in recent decades (on public and private land) because of changing farming practices and increased habitat protections. The increasing availability of large diameter trees, increasing forest biomass, and changing forest compositions have the potential to influence Indiana bat roost habitat preferences. We assessed Indiana bat maternity roost selection at the tree and forest plot scale to characterize patterns of use in this region from 2017–2018. We predicted that large trees on the landscape would support large colonies of Indiana bats. We located bats in multiple species of trees including elm (Ulmus spp.), cottonwood (Populus deltoides), and shagbark hickory (Carya ovata). We documented larger maternity colonies sharing roosts than in previous studies from the 1980s in the same region. We suggest managers and regulatory agencies monitor Indiana bats in dynamic landscapes such as those with changing forest composition and biomass.     

Recruitment-dance signals draw larger audiences when honey bee colonies have multiple patrilines

Honey bee queens (Apis mellifera) who mate with multiple males produce colonies that are filled with numerous genetically distinct patrilines of workers. A genetically diverse colony benefits from an enhanced foraging effort, fuelled in part by an increase in the number of recruitment signals that are produced by foragers. However, the influence of patriline diversity on the attention paid to these signals by audiences of potentially receptive workers remains unexplored. To determine whether recruitment dances performed by foragers in multiple-patriline colonies attract a greater number of dance followers than dances in colonies that lack patriline diversity, we trained workers from multiple- and single-patriline colonies to forage in a greenhouse and monitored their dance-following activity back in the hives. On average, more workers followed a dance if it was performed in a multiple-patriline colony rather than a single-patriline colony (33% increase), and for a greater number of dance circuits per follower. Furthermore, dance-following workers in multiple-patriline colonies were more likely to exit their hive after following a dance, although this did not translate to a difference in colony-level exit rates between treatment types. Recruiting nest mates to profitable food sources through dance communication is critical to a colony’s foraging success and long-term fitness; polyandrous queens produce colonies that benefit not only from increased recruitment signalling, but also from the generation of larger and more attentive audiences of signal receivers. This study highlights the importance of integrating responses of both signal senders and receivers to understand more fully the success of animal-communication systems.     

The within-nest behaviour of honeybee pollen foragers in colonies with a high or low need for pollen

Numerous studies have documented that honeybee colonies can rapidly adjust the number of foragers collecting pollen in response to changes in quantities of brood, pollen and nectar in the nest. However, few studies have examined the behaviour of individual pollen foragers while in the nest between trips. Thus, little is known about how a pollen forager actually assesses its colony's needs. To understand this process better, we observed the behaviour of 319 pollen foragers while in their nests between foraging trips. We observed foragers in two types of nest environments: one with a relatively high need for pollen and one with a relatively low need for pollen. Foragers performed as many as 14 activities during two phases demarcated by the unloading of pollen loads. They inspected empty cells and cells with pollen, and performed the waggle dance at higher relative frequencies before unloading (P≤ 0.0004 each act). They antennated nestmates, autogroomed and received trophallaxis at higher relative frequencies after unloading (P≤ 0.0004 each act). All acts were performed both before and after unloading, but not always by each bee. Pollen foragers discriminated among cells based on cell contents in two contexts. First, they inspected cells already containing pollen more often than expected by chance. Second, their pattern of inspecting cells with different contents differed from their pattern of unloading pollen loads in those cells. Pollen foragers performed 42.3±4.6% (least square mean±SE) of preunloading inspection events on empty cells, but unloaded in them only 19.9±4.6% of the time. They performed 42.2±4.6% of preunloading inspection events on cells already containing pollen, but unloaded in them 79.4±4.6% of the time (P< 0.0001). Our data show that pollen foragers can determine the contents of cells in the nest and suggest that the regulation of pollen collection involves direct assessment of colony need by pollen foragers. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The adaptive value of inactive foragers and the scout-recruit system in honey bee (Apis mellifera) colonies

In honey bee (Apis mellifera) colonies, scouts search for productiveforage sites and then recruit other workers to those locations using a waggle dance. A simple and tractable mathematical modelof the honey bee scout-recruit system was developed to studythe relationship between nectar availability, the efficiencyof the honey bee's recruitment system, and the optimal proportionof scouts that maximizes net gain (benefit - cost), or, energeticefficiency (benefit/cost - 1). The models consider both the energetic costs and benefits of active scouts and recruits aswell as the cost of an inactive forager reserve. They predictconditions when individual foraging is favored over the honeybee's recruitment system, when the colony should abandon foragingaltogether, and the optimal proportion of scouts (when thescout-recruit system is favored). The models' predictions qualitatively match empirical data. Surprisingly, previous empirical datafrom the honey bee suggest that recruits' costs are greaterthan scouts'—recruits spend significantly longer searchingfor a forage patch than do scouts—thereby causing researchersto rethink how the scout-recruit system might be adaptive. Using average returns, the models demonstrate how the scout-recruitsystem is adaptive despite these apparent higher recruit costsrelative to the scouts'. A sensitivity analysis demonstratesthat the results are robust to a broad range of relative costsof active workers, inactive workers, and the energetic benefitsof the forage. Consequently, the model is demonstrated to berelevant to many insect societies that employ a scout-recruitsystem.     

Females produce larger eggs for large males in a paternal mouthbrooding fish.

When individuals receive different returns from their reproductive investment dependent on mate quality, they are expected to invest more when breeding with higher quality mates. A number of studies over the past decade have shown that females may alter their reproductive effort depending on the quality/attractiveness of their mate. However, to date, despite extensive work on parental investment, such a differential allocation has not been demonstrated in fish. Indeed, so far only two studies from any taxon have suggested that females alter the quality of individual offspring according to the quality/attractiveness of their mate. The banggai cardinal fish is an obligate paternal mouth brooder where females lay few large eggs. It has previously been shown that male size determines clutch weight irrespective of female size in this species. In this study, I investigated whether females perform more courtship displays towards larger males and whether females allocate their reproductive effort depending on the size of their mate by experimentally assigning females to either large or small males. I found that females displayed more towards larger males, thereby suggesting a female preference for larger males. Further, females produced heavier eggs and heavier clutches but not more eggs when paired with large males. My experiments show that females in this species adjust their offspring weight and, thus, presumably offspring quality according to the size of their mate.     

Climate refugia and migration requirements in complex landscapes

All of today's species have proven their ability to cope with climate change during the glacial‐interglacial cycles of the Quaternary, but future migration requirements may be different regarding speed, direction, geographic barriers, and availability of nearby climate refugia. Here, we contribute a landscape‐level climatic analysis of postglacial vs. projected future migration requirements for 24 common western North American tree species. Using a recently developed velocity of climate change algorithm, we quantify required migration velocities for all populations of species to track climate habitat, based on projections from general circulation models for the 2080s and the last glacial maximum, 21 000 yr ago. Specifically, we ask if nearby climate refugia exist for at least some populations within species ranges and whether the current landscape position of species imply qualitatively different migration requirements in the future compared to those during glacial‐interglacial cycles. Results showed that velocities to reach the nearest climate refugia in the future still exceed the fastest reconstructed post‐glacial migration requirements, but not by orders of magnitude. Regarding landscape positions, we find a low correlation among past and future migration requirements (r = 0.38), suggesting that qualitatively different migration patterns may emerge in the future for some species. Species identified as occupying landscape positions requiring disproportionally faster migration requirements in the future include whitebark pine, pinyon pine, and coast redwood. We discuss uncertainties of our analytical approach as well as implications for human‐assisted migration and conservation action to address climate change.     

Woody elements benefit bird diversity to a larger extent than semi-natural grasslands in cereal-dominated landscapes

Increasing landscape complexity can mitigate negative effects of agricultural intensification on biodiversity by offering resources complementary to those provided in arable fields. In particular, grazed semi-natural grasslands and woody elements support farmland birds, but little is known about their relative effects on bird diversity and community composition. In addition, the relative importance of local habitat versus landscape composition remains unclear. We investigated how the presence of semi-natural grasslands, the number of woody elements and the composition of the wider agricultural landscape affect bird species richness, true diversity (exponential Shannon diversity) and species composition. Bird communities were surveyed four times on 16 paired transects of 250 m each with 8 transects placed between a crop field and a semi-natural grassland and 8 transects between two crop fields with no semi-natural grasslands in the vicinity. The number of woody elements around transects was selected as an important predictor in all models, having a positive effect on species richness and true diversity, while the local presence of semi-natural grasslands was not selected in the best models. However, species richness and true diversity increased with increasing cover of ley and semi-natural grasslands, whereas species composition was modified by the coverage of winter wheat at the landscape scale. Furthermore, bird species richness, true diversity and species composition differed between sampling dates. As bird diversity benefited from woody elements, rather than from the local presence of semi-natural grasslands as such, it is important to maintain woody structures in farmland. However, the positive effect of grassland at the landscape scale highlights the importance of habitat variability at multiple scales. Because species richness and true diversity were affected by different landscape components compared to species composition, a mosaic of land-use types is needed to achieve multiple conservation goals across agricultural landscapes.     

Red Junglefowl (Gallus gallus) selected for low fear of humans are larger,more dominant and produce larger offspring

Many traits associated with domestication are suggested to have developed as correlated responses to reduced fear of humans. Tameness may have reduced the stress of living in human proximity and improved welfare in captivity. We selected Red Junglefowl (ancestors of all domestic chickens) for four generations on high or low fear towards humans, mimicking an important aspect of the earliest period of domestication, and tested birds from the third and fourth generation in three different social tests. Growth and plumage condition, as well as size of eggs and offspring were also recorded, as indicators of some aspects of welfare. Birds selected for low fear had higher weight, laid larger eggs and generated larger offspring, and had a better plumage condition. In a social dominance test they also performed more aggressive behaviour and received less of the same, regardless of whether the restricted resource was feed or not. Hence, dominance appeared to increase as a consequence of reduced fear of humans. Furthermore, egg size and the weight of the offspring were larger in the less fearful birds, and plumage condition better, which could be interpreted as the less fearful animals being better adapted to the environment in which they were selected.     

Rugged adaptive landscapes shape a complex,sympatric radiation

Strong disruptive ecological selection can initiate speciation, even in the absence of physical isolation of diverging populations. Species evolving under disruptive ecological selection are expected to be ecologically distinct but, at least initially, genetically weakly differentiated. Strong selection and the associated fitness advantages of narrowly adapted individuals, coupled with assortative mating, are predicted to overcome the homogenizing effects of gene flow. Theoretical plausibility is, however, contrasted by limited evidence for the existence of rugged adaptive landscapes in nature. We found evidence for multiple, disruptive ecological selection regimes that have promoted divergence in the sympatric, incipient radiation of ‘sharpfin’ sailfin silverside fishes in ancient Lake Matano (Sulawesi, Indonesia). Various modes of ecological specialization have led to adaptive morphological differences between the species, and differently adapted morphs display significant but incomplete reproductive isolation. Individual fitness and variation in morphological key characters show that disruptive selection shapes a rugged adaptive landscape in this small but complex incipient lake fish radiation.     

Evolutionary advantage of small populations on complex fitness landscapes

Recent experimental and theoretical studies have shown that small asexual populations evolving on complex fitness landscapes may achieve a higher fitness than large ones due to the increased heterogeneity of adaptive trajectories. Here, we introduce a class of haploid three-locus fitness landscapes that allow the investigation of this scenario in a precise and quantitative way. Our main result derived analytically shows how the probability of choosing the path of the largest initial fitness increase grows with the population size. This makes large populations more likely to get trapped at local fitness peaks and implies an advantage of small populations at intermediate time scales. The range of population sizes where this effect is operative coincides with the onset of clonal interference. Additional studies using ensembles of random fitness landscapes show that the results achieved for a particular choice of three-locus landscape parameters are robust and also persist as the number of loci increases. Our study indicates that an advantage for small populations is likely whenever the fitness landscape contains local maxima. The advantage appears at intermediate time scales, which are long enough for trapping at local fitness maxima to have occurred but too short for peak escape by the creation of multiple mutants.     

Crystallographic refinement by knowledge-based exploration of complex energy landscapes

Although X-ray crystallography remains the most versatile method to determine the three-dimensional atomic structure of proteins and much progress has been made in model building and refinement techniques, it remains a challenge to elucidate accurately the structure of proteins in medium-resolution crystals. This is largely due to the difficulty of exploring an immense conformational space to identify the set of conformers that collectively best fits the experimental diffraction pattern. We show here that combining knowledge-based conformational sampling in RAPPER with molecular dynamics/simulated annealing (MD/SA) vastly improves the quality and power of refinement compared to MD/SA alone. The utility of this approach is highlighted by the automated determination of a lysozyme mutant from a molecular replacement solution that is in congruence with a model prepared independently by crystallographers. Finally, we discuss the implications of this work on structure determination in particular and conformational sampling and energy minimization in general.     

Prey processing in central place foragers

The importance of prey processing as an integral part of foraging behaviour has long been acknowledged, but little theoretical consideration has been given to the optimization of the processing behaviour itself. Processing renders food down to ingestible, palatable portions, and also removes non-essential mass thus reducing transport costs. Here, several models of processing are developed for a central place forager. When the forager has to make a simple choice between processing the prey and not, a critical distance from the central place can be calculated, beyond which it is optimal to process prey. If the forager also decides on how much of the prey to remove, the optimal amount to be removed can also be calculated. Imposing a ceiling on overall metabolic expenditure is shown to reduce the distances at which processing becomes the optimal strategy. The models are tested using parameters derived for a provisioning merlin, Falco columbarius, and alternative explanations as to why observed behaviours should differ from the optimal behaviour predicted are discussed.     

Heterogeneous adaptive trajectories of small populations on complex fitness landscapes

Background

Small populations are thought to be adaptively handicapped, not only because they suffer more from deleterious mutations but also because they have limited access to new beneficial mutations, particularly those conferring large benefits.

Methodology/Principal Findings

Here, we test this widely held conjecture using both simulations and experiments with small and large bacterial populations evolving in either a simple or a complex nutrient environment. Consistent with expectations, we find that small populations are adaptively constrained in the simple environment; however, in the complex environment small populations not only follow more heterogeneous adaptive trajectories, but can also attain higher fitness than the large populations. Large populations are constrained to near deterministic fixation of rare large-benefit mutations. While such determinism speeds adaptation on the smooth adaptive landscape represented by the simple environment, it can limit the ability of large populations from effectively exploring the underlying topography of rugged adaptive landscapes characterized by complex environments.

Conclusions

Our results show that adaptive constraints often faced by small populations can be circumvented during evolution on rugged adaptive landscapes.