Environmental harshness does not affect the propensity for social learning in great tits, Parus major.

According to the harsh environment hypothesis, natural selection should favour cognitive mechanisms to overcome environmental challenges. Tests of this hypothesis to date have largely focused on asocial learning and memory, thus failing to account for the spread of information via social means. Tests in specialized food-hoarding birds have shown strong support for the effects of environmental harshness on both asocial and social learning. Whether the hypothesis applies to non-specialist foraging species remains largely unexplored. We evaluated the relative importance of social learning across a known harshness gradient by testing generalist great tits, Parus major, from high (harsh)- and low (mild)-elevation populations in two social learning tasks. We showed that individuals use social learning to find food in both colour-associative and spatial foraging tasks and that individuals differed consistently in their use of social learning. However, we did not detect a difference in the use or speed of implementing socially observed information across the elevational gradient. Our results do not support predictions of the harsh environment hypothesis suggesting that context-dependent costs and benefits as well as plasticity in the use of social information may play an important role in the use of social learning across environments. Finally, this study adds to the accumulating evidence that the harsh environment hypothesis appears to have more pronounced effects on specialists compared to generalist species.

Loss of flockmates weakens winter site fidelity in golden-crowned sparrows (Zonotrichia atricapilla).

Animal social interactions have an intrinsic spatial basis as many of these interactions occur in spatial proximity. This presents a dilemma when determining causality: Do individuals interact socially because they happen to share space, or do they share space because they are socially linked? We present a method that uses demographic turnover events as a natural experiment to investigate the links between social associations and space use in the context of interannual winter site fidelity in a migratory bird. We previously found that golden-crowned sparrows (Zonotrichia atricapilla) show consistent flocking relationships across years, and that familiarity between individuals influences the dynamics of social competition over resources. Using long-term data on winter social and spatial behavior across 10 y, we show that i) sparrows exhibit interannual fidelity to winter home ranges on the scale of tens of meters and ii) the precision of interannual site fidelity increases with the number of winters spent, but iii) this fidelity is weakened when sparrows lose close flockmates from the previous year. Furthermore, the effect of flockmate loss on site fidelity was higher for birds that had returned in more than 2 winters, suggesting that social fidelity may play an increasingly important role on spatial behavior across the lifetime of this migratory bird. Our study provides evidence that social relationships can influence site fidelity, and shows the potential of long-term studies for disentangling the relationship between social and spatial behavior.

Parasite detection and quantification in avian blood is dependent on storage medium and duration.

Studies of parasites in wild animal populations often rely on molecular methods to both detect and quantify infections. However, method accuracy is likely to be influenced by the sampling approach taken prior to nucleic acid extraction. Avian Haemosporidia are studied primarily through the screening of host blood, and a range of storage mediums are available for the short- to long-term preservation of samples. Previous research has suggested that storage medium choice may impact the accuracy of PCR-based parasite detection, however, this relationship has never been explicitly tested and may be exacerbated by the duration of sample storage. These considerations could also be especially critical for sensitive molecular methods used to quantify infection (qPCR). To test the effect of storage medium and duration on Plasmodium detection and quantification, we split blood samples collected from wild birds across three medium types (filter paper, Queen's lysis buffer, and 96% ethanol) and carried out DNA extractions at five time points (1, 6, 12, 24, and 36 months post-sampling). First, we found variation in DNA yield obtained from blood samples dependent on their storage medium which had subsequent negative impacts on both detection and estimates of Plasmodium copy number. Second, we found that detection accuracy (incidence of true positives) was highest for filter-paper-stored samples (97%), while accuracy for ethanol and Queen's lysis buffer-stored samples was influenced by either storage duration or extraction yield, respectively. Lastly, longer storage durations were associated with decreased copy number estimates across all storage mediums; equating to a 58% reduction between the first- and third-year post-sampling for lysis-stored samples. These results raise questions regarding the utility of standardizing samples by dilution, while also illustrating the critical importance of considering storage approaches in studies of Haemosporidia comparing samples subjected to different storage regimes and/or stored for varying lengths of time.

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird.

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.

Dispersal plasticity driven by variation in fitness across species and environmental gradients.

Dispersal plasticity, when organisms adjust their dispersal decisions depending on their environment, can play a major role in ecological and evolutionary dynamics, but how it relates to fitness remains scarcely explored. Theory predicts that high dispersal plasticity should evolve when environmental gradients have a strong impact on fitness. Using microcosms, we tested in five species of the genus Tetrahymena whether dispersal plasticity relates to differences in fitness sensitivity along three environmental gradients. Dispersal plasticity was species- and environment-dependent. As expected, dispersal plasticity was generally related to fitness sensitivity, with higher dispersal plasticity when fitness is more affected by environmental gradients. Individuals often preferentially disperse out of low fitness environments, but leaving environments that should yield high fitness was also commonly observed. We provide empirical support for a fundamental, but largely untested, assumption in dispersal theory: the extent of dispersal plasticity correlates with fitness sensitivity to the environment.

Dispersal syndromes in challenging environments: A cross-species experiment.

Dispersal is a central biological process tightly integrated into life-histories, morphology, physiology and behaviour. Such associations, or syndromes, are anticipated to impact the eco-evolutionary dynamics of spatially structured populations, and cascade into ecosystem processes. As for dispersal on its own, these syndromes are likely neither fixed nor random, but conditional on the experienced environment. We experimentally studied how dispersal propensity varies with individuals' phenotype and local environmental harshness using 15 species ranging from protists to vertebrates. We reveal a general phenotypic dispersal syndrome across studied species, with dispersers being larger, more active and having a marked locomotion-oriented morphology and a strengthening of the link between dispersal and some phenotypic traits with environmental harshness. Our proof-of-concept metacommunity model further reveals cascading effects of context-dependent syndromes on the local and regional organisation of functional diversity. Our study opens new avenues to advance our understanding of the functioning of spatially structured populations, communities and ecosystems.

Evidence of attack deflection suggests adaptive evolution of wing tails in butterflies.

Predation is a powerful selective force shaping many behavioural and morphological traits in prey species. The deflection of predator attacks from vital parts of the prey usually involves the coordinated evolution of prey body shape and colour. Here, we test the deflection effect of hindwing (HW) tails in the swallowtail butterfly Iphiclides podalirius. In this species, HWs display long tails associated with a conspicuous colour pattern. By surveying the wings within a wild population of I. podalirius, we observed that wing damage was much more frequent on the tails. We then used a standardized behavioural assay employing dummy butterflies with real I. podalirius wings to study the location of attacks by great tits Parus major. Wing tails and conspicuous coloration of the HWs were struck more often than the rest of the body by birds. Finally, we characterized the mechanical properties of fresh wings and found that the tail vein was more fragile than the others, suggesting facilitated escape ability of butterflies attacked at this location. Our results clearly support the deflective effect of HW tails and suggest that predation is an important selective driver of the evolution of wing tails and colour pattern in butterflies.

Great tits who remember more accurately have difficulty forgetting, but variation is not driven by environmental harshness.

The causes of individual variation in memory are poorly understood in wild animals. Harsh environments with sparse or rapidly changing food resources are hypothesized to favour more accurate spatial memory to allow animals to return to previously visited patches when current patches are depleted. A potential cost of more accurate spatial memory is proactive interference, where accurate memories block the formation of new memories. This relationship between spatial memory, proactive interference, and harsh environments has only been studied in scatter-hoarding animals. We compare spatial memory accuracy and proactive interference performance of non-scatter hoarding great tits (Parus major) from high and low elevations where harshness increases with elevation. In contrast to studies of scatter-hoarders, we did not find a significant difference between high and low elevation birds in their spatial memory accuracy or proactive interference performance. Using a variance partitioning approach, we report the first among-individual trade-off between spatial memory and proactive interference, uncovering variation in memory at the individual level where selection may act. Although we have no evidence of harsh habitats affecting spatial memory, our results suggest that if elevation produced differences in spatial memory between elevations, we could see concurrent changes in how quickly birds can forget.

Schoolchildren cooperate more successfully with non-kin than with siblings.

Cooperation plays a key role in the development of advanced societies and can be stabilized through shared genes (kinship) or reciprocation. In humans, cooperation among kin occurs more readily than cooperation among non-kin. In many organisms, cooperation can shift with age (e.g. helpers at the nest); however, little is known about developmental shifts between kin and non-kin cooperation in humans. Using a cooperative game, we show that 3- to 10-year-old French schoolchildren cooperated less successfully with siblings than with non-kin children, whether or not non-kin partners were friends. Furthermore, children with larger social networks cooperated better and the perception of friendship among non-friends improved after cooperating. These results contrast with the well-established preference for kin cooperation among adults and indicate that non-kin cooperation in humans might serve to forge and extend non-kin social relationships during middle childhood and create opportunities for future collaboration beyond kin. Our results suggest that the current view of cooperation in humans may only apply to adults and that future studies should focus on how and why cooperation with different classes of partners might change during development in humans across cultures as well as other long-lived organisms.

Social Evolution: Big Benefits of BFFs.

Having long-term familiar neighbors - rather than kin neighbors - can increase survival and double reproductive success in North American red squirrels. These benefits are so high they can slow senescence and may explain numerous social behaviors in this otherwise individualistic species.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co-occurring host species.

Understanding the ecology and evolution of parasites is contingent on identifying the selection pressures they face across their infection landscape. Such a task is made challenging by the fact that these pressures will likely vary across time and space, as a result of seasonal and geographical differences in host susceptibility or transmission opportunities. Avian haemosporidian blood parasites are capable of infecting multiple co-occurring hosts within their ranges, yet whether their distribution across time and space varies similarly in their different host species remains unclear. Here, we applied a new PCR method to detect avian haemosporidia (genera Haemoproteus, Leucocytozoon, and Plasmodium) and to determine parasite prevalence in two closely related and co-occurring host species, blue tits (Cyanistes caeruleus, N = 529) and great tits (Parus major, N = 443). Our samples were collected between autumn and spring, along an elevational gradient in the French Pyrenees and over a three-year period. Most parasites were found to infect both host species, and while these generalist parasites displayed similar elevational patterns of prevalence in the two host species, this was not always the case for seasonal prevalence patterns. For example, Leucocytozoon group A parasites showed inverse seasonal prevalence when comparing between the two host species, being highest in winter and spring in blue tits but higher in autumn in great tits. While Plasmodium relictum prevalence was overall lower in spring relative to winter or autumn in both species, spring prevalence was also lower in blue tits than in great tits. Together, these results reveal how generalist parasites can exhibit host-specific epidemiology, which is likely to complicate predictions of host-parasite co-evolution.

Social Games and Genic Selection Drive Mammalian Mating System Evolution and Speciation.

Mating system theory based on economics of resource defense has been applied to describe social system diversity across taxa. Such models are generally successful but fail to account for stable mating systems across different environments or shifts in mating system without a change in ecological conditions. We propose an alternative approach to resource defense theory based on frequency-dependent competition among genetically determined alternative behavioral strategies characterizing many social systems (polygyny, monogamy, sneak). We modeled payoffs for competition, neighborhood choice, and paternal care to determine evolutionary transitions among mating systems. Our model predicts four stable outcomes driven by the balance between cooperative and agonistic behaviors: promiscuity (two or three strategies), polygyny, and monogamy. Phylogenetic analysis of 288 rodent species supports assumptions of our model and is consistent with patterns of evolutionarily stable states and mating system transitions. Support for model assumptions include that monogamy and polygyny evolve from promiscuity and that paternal care and monogamy are coadapted in rodents. As predicted by our model, monogamy and polygyny occur in sister taxa among rodents more often than by chance. Transitions to monogamy also favor higher speciation rates in subsequent lineages, relative to polygynous sister lineages. Taken together, our results suggest that genetically based neighborhood choice behavior and paternal care can drive transitions in mating system evolution. While our genic mating system theory could complement resource-based theory, it can explain mating system transitions regardless of resource distribution and provides alternative explanations, such as evolutionary inertia, when resource ecology and mating systems do not match.

Variability in Dispersal Syndromes Is a Key Driver of Metapopulation Dynamics in Experimental Microcosms.

Evolutionary ecology studies have increasingly focused on the impact of intraspecific variability on population processes. However, the role such variation plays in the dynamics of spatially structured populations and how it interacts with environmental changes remains unclear. Here we experimentally quantify the relative importance of intraspecific variability in dispersal-related traits and spatiotemporal variability of environmental conditions for the dynamics of two-patch metapopulations using clonal genotypes of a ciliate in connected microcosms. We demonstrate that in our simple two-patch microcosms, differences among genotypes are at least as important as spatiotemporal variability of resources for metapopulation dynamics. Furthermore, we show that an important proportion of this effect results from variability of dispersal syndromes. These syndromes can therefore be as important for metapopulation dynamics as spatiotemporal variability of environmental conditions. This study demonstrates that intraspecific variability in dispersal syndromes can be key in the functioning of metapopulations facing environmental changes.

Experimentally induced increases in fecundity lead to greater nestling care in blue tits.

Models on the evolution of bi-parental care typically assume that maternal investment in offspring production is fixed and predict subsequent contributions to offspring care by the pair are stabilized by partial compensation. While experimental tests of this prediction are supportive, exceptions are commonplace. Using wild blue tits ( Cyanistes caeruleus), we provide, to our knowledge, the first investigation into the effects of increasing maternal investment in offspring production for subsequent contributions to nestling provisioning by mothers and male partners. Females that were induced to lay two extra eggs provisioned nestlings 43% more frequently than controls, despite clutch size being made comparable between treatment groups at the onset of incubation. Further, experimental males did not significantly reduce provisioning rates as expected by partial compensation, and if anything contributed slightly (9%) more than controls. Finally, nestlings were significantly heavier in experimental nests compared with controls, suggesting that the 22% average increase in provisioning rates by experimental pairs was beneficial. Our results have potential implications for our understanding of provisioning rules, the maintenance of bi-parental care and the timescale over which current-future life-history trade-offs operate. We recommend greater consideration of female investment at the egg stage to more fully understand the evolutionary dynamics of bi-parental care.

Habitat choice meets thermal specialization: Competition with specialists may drive suboptimal habitat preferences in generalists.

Limited dispersal is classically considered as a prerequisite for ecological specialization to evolve, such that generalists are expected to show greater dispersal propensity compared with specialists. However, when individuals choose habitats that maximize their performance instead of dispersing randomly, theory predicts dispersal with habitat choice to evolve in specialists, while generalists should disperse more randomly. We tested whether habitat choice is associated with thermal niche specialization using microcosms of the ciliate Tetrahymena thermophila, a species that performs active dispersal. We found that thermal specialists preferred optimal habitats as predicted by theory, a link that should make specialists more likely to track suitable conditions under environmental changes than expected under the random dispersal assumption. Surprisingly, generalists also performed habitat choice but with a preference for suboptimal habitats. Since this result challenges current theory, we developed a metapopulation model to understand under which circumstances such a preference for suboptimal habitats should evolve. We showed that competition between generalists and specialists may favor a preference for niche margins in generalists under environmental variability. Our results demonstrate that the behavioral dimension of dispersal-here, habitat choice-fundamentally alters our predictions of how dispersal evolve with niche specialization, making dispersal behaviors crucial for ecological forecasting facing environmental changes.

Bottom-up and top-down control of dispersal across major organismal groups.

Ecology and evolution unfold in spatially structured communities, where dispersal links dynamics across scales. Because dispersal is multicausal, identifying general drivers remains challenging. In a coordinated distributed experiment spanning organisms from protozoa to vertebrates, we tested whether two fundamental determinants of local dynamics, top-down and bottom-up control, generally explain active dispersal. We show that both factors consistently increased emigration rates and use metacommunity modelling to highlight consequences on local and regional dynamics.

Manipulating badges of status only fools strangers.

Conflict is risky, but mechanisms that allow animals to assess dominance status without aggression can reduce such costs. Two different mechanisms of competitor assessment are expected to evolve in different contexts: badges of status are expected in larger, anonymous groups, whereas individual recognition is feasible in small, stable groups. However, both mechanisms may be important when social interactions occur both within and across stable social groups. We manipulated plumage in golden-crowned sparrows (Zonotrichia atricapilla) and found that two known badges of status - gold and black head plumage patch sizes - independently affect dominance among strangers but manipulations had no effect on dominance among familiar flockmates. Moreover, familiar flockmates showed less aggression and increased foraging relative to strangers. Our study provides clear experimental evidence that social recognition affects badge function, and suggests that variation in social contexts maintains coexistence and context-dependent use of these two dominance resolution mechanisms.

Chemical regulation of body feather microbiota in a wild bird.

The microbiota has a broad range of impacts on host physiology and behaviour, pointing out the need to improve our comprehension of the drivers of host-microbiota composition. Of particular interest is whether the microbiota is acquired passively, or whether and to what extent hosts themselves shape the acquisition and maintenance of their microbiota. In birds, the uropygial gland produces oily secretions used to coat feathers that have been suggested to act as an antimicrobial defence mechanism regulating body feather microbiota. However, our comprehension of this process is still limited. In this study, we for the first time coupled high-throughput sequencing of the microbiota of both body feathers and the direct environment (i.e., the nest) in great tits with chemical analyses of the composition of uropygial gland secretions to examine whether host chemicals have either specific effects on some bacteria or nonspecific broad-spectrum effects on the body feather microbiota. Using a network approach investigating the patterns of co-occurrence or co-exclusions between chemicals and bacteria within the body feather microbiota, we found no evidence for specific promicrobial or antimicrobial effects of uropygial gland chemicals. However, we found that one group of chemicals was negatively correlated to bacterial richness on body feathers, and a higher production of these chemicals was associated with a poorer body feather bacterial richness compared to the nest microbiota. Our study provides evidence that chemicals produced by the host might function as a nonspecific broad-spectrum antimicrobial defence mechanism limiting colonization and/or maintenance of bacteria on body feathers, providing new insight about the drivers of the host's microbiota composition in wild organisms.

The roles of plasticity versus dominance in maintaining polymorphism in mating strategies.

Although natural selection is expected to reduce variability, polymorphism is common in nature even under strong selective regimes. Discrete polymorphisms in mating strategies are widespread and offer a good opportunity to understand the genetic processes that allow the maintenance of polymorphism in relatively simple systems. Here we explored the genetic mechanism underlying the expression of discrete mating strategies in the rock-paper-scissors (RPS) game. Heterozygotes carry the genetic information for two different strategies, yet little attention has been devoted to the mechanisms underpinning heterozygote phenotype and its consequences for allele frequency dynamics. We explored the maintenance of polymorphism under 1) genetic dominance or 2) plasticity, as mechanisms driving the expression of alternative strategies in males. We developed an alternative mating strategy model and analysed allele frequency dynamics using time series analyses. Our results show that both genetic mechanisms can maintain polymorphism depending on population demographic characteristics but that plasticity can enhance the likelihood that polymorphism is maintained relative to dominance. Time series analysis on simulation outcomes show that the RPS game is mostly driven by a single strategy, but the importance of this strategy on long term dynamics is stronger when gene expression shows dominance rather than plasticity.