The effect of environmental variation on the relationship between survival and risk-taking behaviour in a migratory songbird.

Temporal changes in environmental conditions may play a major role in the year-to-year variation in fitness consequences of behaviours. Identifying environmental drivers of such variation is crucial to understand the evolutionary trajectories of behaviours in natural contexts. However, our understanding of how environmental variation influences behaviours in the wild remains limited. Using data collected over 14 breeding seasons from a collared flycatcher (Ficedula albicollis) population, we examined the effect of environmental variation on the relationship between survival and risk-taking behaviour, a highly variable behavioural trait with great evolutionary and ecological significance. Specifically, using annual recapture probability as a proxy of survival, we evaluated the specific effect of predation pressure, food availability, and mean temperature on the relationship between annual recapture probability and risk-taking behaviour (measured as flight initiation distance [FID]). We found a negative trend, as the relationship between annual recapture probability and FID decreased over the study years and changed from positive to negative. Specifically, in the early years of the study, risk-avoiding individuals exhibited a higher annual recapture probability, whereas in the later years, risk-avoiders had a lower annual recapture probability. However, we did not find evidence that any of the considered environmental factors mediated the variation in the relationship between survival and risk-taking behaviour.

The estimation of additive genetic variance of body size in a wild passerine is sensitive to the method used to estimate relatedness among the individuals.

Assessing additive genetic variance is a crucial step in predicting the evolutionary response of a target trait. However, the estimated genetic variance may be sensitive to the methodology used, e.g., the way relatedness is assessed among the individuals, especially in wild populations where social pedigrees can be inaccurate. To investigate this possibility, we investigated the additive genetic variance in tarsus length, a major proxy of skeletal body size in birds. The model species was the collared flycatcher (Ficedula albicollis), a socially monogamous but genetically polygamous migratory passerine. We used two relatedness matrices to estimate the genetic variance: (1) based solely on social links and (2) a genetic similarity matrix based on a large array of single-nucleotide polymorphisms (SNPs). Depending on the relatedness matrix considered, we found moderate to high additive genetic variance and heritability estimates for tarsus length. In particular, the heritability estimates were higher when obtained with the genetic similarity matrix instead of the social pedigree. Our results confirm the potential for this crucial trait to respond to selection and highlight methodological concerns when calculating additive genetic variance and heritability in phenotypic traits. We conclude that using a social pedigree instead of a genetic similarity matrix to estimate relatedness among individuals in a genetically polygamous wild population may significantly deflate the estimates of additive genetic variation.

Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species.

Comprehending symbiont abundance among host species is a major ecological endeavour, and the metabolic theory of ecology has been proposed to understand what constrains symbiont populations. We parameterized metabolic theory equations to investigate how bird species' body size and the body size of their feather mites relate to mite abundance according to four potential energy (uropygial gland size) and space constraints (wing area, total length of barbs and number of feather barbs). Predictions were compared with the empirical scaling of feather mite abundance across 106 passerine bird species (26,604 individual birds sampled), using phylogenetic modelling and quantile regression. Feather mite abundance was strongly constrained by host space (number of feather barbs) but not by energy. Moreover, feather mite species' body size was unrelated to the body size of their host species. We discuss the implications of our results for our understanding of the bird-feather mite system and for symbiont abundance in general.

Phylogenetic meta-analysis reveals system-specific behavioural type-behavioural predictability correlations.

The biological significance of behavioural predictability (environment-independent within-individual behavioural variation) became accepted recently as an important part of an individual's behavioural strategy besides behavioural type (individual mean behaviour). However, we do not know how behavioural type and predictability evolve. Here, we tested different evolutionary scenarios: (i) the two traits evolve independently (lack of correlations) and (ii) the two traits' evolution is constrained (abundant correlations) due to either (ii/a) proximate constraints (direction of correlations is similar) or (ii/b) local adaptations (direction of correlations is variable). We applied a set of phylogenetic meta-analyses based on 93 effect sizes across 44 vertebrate and invertebrate species, focusing on activity and risk-taking. The general correlation between behavioural type and predictability did not differ from zero. Effect sizes for correlations showed considerable heterogeneity, with both negative and positive correlations occurring. The overall absolute (unsigned) effect size was high (Zr = 0.58), and significantly exceeded the null expectation based on randomized data. Our results support the adaptive scenario: correlations between behavioural type and predictability are abundant in nature, but their direction is variable. We suggest that the evolution of these behavioural components might be constrained in a system-specific way.

Using community science data to assess the association between urbanization and the presence of invasive Aedes species in Hungary.

BACKGROUND: Urbanization can be a significant contributor to the spread of invasive mosquito vector species, and the diseases they carry, as urbanized habitats provide access to a great density of food resources (humans and domestic animals) and offer abundant breeding sites for these vectors. Although anthropogenic landscapes are often associated with the presence of invasive mosquito species, we still have little understanding about the relationships between some of these and the built environment. METHODS: This study explores the association between urbanization level and the occurrence of invasive Aedes species, specifically Aedes albopictus, Aedes japonicus, and Aedes koreicus, in Hungary, using data from a community (or citizen) science program undertaken between 2019 and 2022. RESULTS: The association between each of these species and urbanized landscapes within an extensive geographic area was found to differ. Using the same standardized approach, Ae. albopictus showed a statistically significant and positive relationship with urbanization, whereas Ae. japonicus and Ae. koreicus did not. CONCLUSIONS: The findings highlight the importance of community science to mosquito research, as the data gathered using this approach can be used to make qualitative comparisons between species to explore their ecological requirements.

Evolution of relative brain size in dogs-no effects of selection for breed function, litter size, or longevity.

Domestication is a well-known example of the relaxation of environmentally based cognitive selection that leads to reductions in brain size. However, little is known about how brain size evolves after domestication and whether subsequent directional/artificial selection can compensate for domestication effects. The first animal to be domesticated was the dog, and recent directional breeding generated the extensive phenotypic variation among breeds we observe today. Here we use a novel endocranial dataset based on high-resolution CT scans to estimate brain size in 159 dog breeds and analyze how relative brain size varies across breeds in relation to functional selection, longevity, and litter size. In our analyses, we controlled for potential confounding factors such as common descent, gene flow, body size, and skull shape. We found that dogs have consistently smaller relative brain size than wolves supporting the domestication effect, but breeds that are more distantly related to wolves have relatively larger brains than breeds that are more closely related to wolves. Neither functional category, skull shape, longevity, nor litter size was associated with relative brain size, which implies that selection for performing specific tasks, morphology, and life history does not necessarily influence brain size evolution in domesticated species.

Individual differences in song plasticity in response to social stimuli and singing position.

Individual animals can react to the changes in their environment by exhibiting behaviors in an individual-specific way leading to individual differences in phenotypic plasticity. However, the effect of multiple environmental factors on multiple traits is rarely tested. Such a complex approach is necessary to assess the generality of plasticity and to understand how among-individual differences in the ability to adapt to changing environments evolve. This study examined whether individuals adjust different song traits to varying environmental conditions in the collared flycatcher (Ficedula albicollis), a passerine with complex song. We also aimed to reveal among-individual differences in behavioral responses by testing whether individual differences in plasticity were repeatable. The presence of general plasticity across traits and/or contexts was also tested. To assess plasticity, we documented (1) short-scale temporal changes in song traits in different social contexts (after exposition to male stimulus, female stimulus or without stimuli), and (2) changes concerning the height from where the bird sang (singing position), used as a proxy of predation risk and acoustic transmission conditions. We found population-level relationships between singing position and both song length (SL) and complexity, as well as social context-dependent temporal changes in SL and maximum frequency (MF). We found among-individual differences in plasticity of SL and MF along both the temporal and positional gradients. These among-individual differences in plasticity were repeatable. Some of the plastic responses correlated across different song traits and environmental gradients. Overall, our results show that the plasticity of bird song (1) depends on the social context, (2) exists along different environmental gradients, and (3) there is evidence for trade-offs between the responses of different traits to different environmental variables. Our results highlight the need to consider individual differences and to investigate multiple traits along multiple environmental axes when studying behavioral plasticity.

Experimental evolution reveals differential evolutionary trajectories in male and female activity levels in response to sexual selection and metapopulation structure.

Behavior is central to interactions with the environment and thus has significant consequences for individual fitness. Sexual selection and demographic processes have been shown to independently shape behavioral evolution. Although some studies have tested the simultaneous effects of these forces, no studies have investigated their interplay in behavioral evolution. We applied experimental evolution in the seed beetle Callosobruchus maculatus to investigate, for the first time, the interactive effects of sexual selection intensity (high [polygamy] vs. minimal [enforced monogamy]) and metapopulation structure (yes/no) on the evolution of movement activity, a crucial behavior involved in multiples functions (e.g., dispersal, predator avoidance, or resource acquisition) and thus, closely related to fitness. We found that the interactive effects of the selection regimes did not affect individual activity, which was assayed under two different environments (absence vs. presence of conspecific cues from both sexes). However, contrasting selection regimes led to sex- and context-dependent divergence in activity. The relaxation of sexual selection favored an increase in female, but not male, movement activity that was consistent between environmental contexts. In contrast, selection associated with the presence/absence of metapopulation structure led to context-dependent responses only in male activity. In environments containing cues from conspecifics, males from selection lines under population subdivision showed increased levels of activity compared to those assayed in an environment devoid of conspecifics cues, whereas the opposite was true for males from panmictic lines. These results underscore that both the effects of sexual selection and population spatial structure may be crucial in shaping sex-specific behavioral evolution.

Ecological Predictors of Human Malaria Risk During Different Phases of the Elimination: An Analysis of Historical Data.

To understand the evolutionary ecology of disease dynamics, it is crucial to identify the environmental factors that mediate the spread and abundance of parasites and their vectors. However, human-mediated changes in the biotic and abiotic environment and intervention programs are intensifying in the past 30-40 years at a rate that masks the causal effect of the original ecological predictors. In this study, we used archived epidemiological data spanning over 100 years on malaria risk in Hungary to demonstrate that different associations exist between infection risk and environmental predictors during different phases of the elimination program. In the early 20th century, when malaria was quite common in the country and no defense program was operating, as predicted, there was a positive relationship between the area of flooded habitats and the intensity of malaria infection. In contrast, this relationship was absent during middle of the century, when an effective elimination program was already in effect. Furthermore, malaria morbidity in a given year was predicted by the degree of stagnant water cover of the previous year when considering the period before the launch of a drastic mosquito control program by dichloro-diphenyl-trichloroethane (DDT), whereas such relationship could not be revealed for a latter period. Our results highlight that human-induced alterations of the socioecological environment considerably reorganizes the ecological landscape of pathogens and their vectors.

High frequency of social polygyny reveals little costs for females in a songbird.

Mating system theory predicts that social polygyny-when one male forms pair bonds with two females-may evolve by female choice in species with biparental care. Females will accept a polygynous male if the benefit of mating with a male providing high-quality genes or rearing resources outweighs the cost of sharing mate assistance in parental care. Based on this rationale, we hypothesise that the population frequency of social polygyny (FSP) varies due to changes in mate sharing costs caused by changing environmental conditions. We predicted that: (1) polygamous females (i.e. mated with a polygynous male) pay a survival cost compared to monogamous females; (2) FSP would be higher in years with better rearing conditions and (3) the difference in survival rates between monogamous and polygamous females would be small following years with higher FSP. We tested these predictions using regression and multistate analyses of capture-recapture data of pied flycatchers, Ficedula hypoleuca, in central Spain collected over 26 years (1990-2016). Monogamous females had a higher mean survival rate than polygamous females (prediction 1), but there was no difference in survival between polygynous and monogamous males. In addition, FSP was positively associated with annual reproductive success (a proxy of the quality of rearing conditions-prediction 2). Finally, following years with high FSP, the survival of polygamous females was similar to that of monogamous females (prediction 3), while the chance of breeding in a polygamous state for 2 years in a row increased for both males and females. Our findings suggest that fluctuating environmental conditions may be a necessary but neglected aspect of understanding social polygyny mechanisms.

The effect of social environment on bird song: listener-specific expression of a sexual signal.

Animal signals should consistently differ among individuals to convey distinguishable information about the signalers. However, behavioral display signals, such as bird song are also loaded with considerable within-individual variance with mostly unknown function. We hypothesized that the immediate social environment may play a role in mediating such variance component, and investigated in the collared flycatcher (Ficedula albicollis) if the identity and quality of listeners could affect song production in signalers. After presenting territorial males with either a female or male social stimulus, we found in the subsequent song recordings that the among-stimulus effects corresponded to non-zero variance components in several acoustic traits indicating that singing males are able to plastically adjust their songs according to stimulus identity. Male and female stimuli elicited different responses as the identity of the female stimuli affected song complexity only, while the identity of male stimuli altered also song length, maximum frequency, and song rate. The stimulus-specific effect on song in some cases decreased with time, being particularly detectable right after the removal of the stimulus and ceasing later, but this pattern varied across the sex of the stimulus and the song traits. We were able to identify factors that can explain the among-stimulus effects (e.g., size and quality of the stimuli) with roles that also varied among song traits. Our results confirm that the variable social environment can raise considerable variation in song performance, highlighting that within-individual plasticity of bird song can play important roles in sexual signaling.

Improving the Management of Patients with Osteoporosis Undergoing Spinal Fusion: The Need for a Bone Mineral Density-Matched Interbody Cage.

With an increasingly aging population globally, a confluence has emerged between the rising prevalence of degenerative spinal disease and osteoporosis. Fusion of the anterior spinal column remains the mainstay surgical intervention for many spinal degenerative disorders. However, decreased vertebral bone mineral density (BMD), quantitatively measured by dual x-ray absorptiometry (DXA), complicates treatment with surgical interbody fusion as weak underlying bone stock increases the risk of post-operative implant-related adverse events, including cage subsidence. There is a necessity for developing cages with advanced structural designs that incorporate bioengineering and architectural principles to tailor the interbody fusion device directly to the patient's BMD status. Specifically, lattice-designed cages that mimic the web-like structure of native cancellous bone have demonstrated excellent resistance to post-operative subsidence. This article provides an introductory profile of a spinal interbody implant designed intentionally to simulate the lattice structure of human cancellous bone, with a similar modulus of elasticity, and specialized to match a patient's bone status across the BMD continuum. The implant incorporates an open pore design where the degree of pore compactness directly corresponds to the patient's DXA-defined BMD status, including patients with osteoporosis.

Sequential organization of birdsong: relationships with individual quality and fitness.

Many vocalizing animals produce the discrete elements of their acoustic signals in a specific sequential order, but we know little about the biological relevance of this ordering. For that, we must characterize the degree by which individuals differ in how they organize their signals sequentially and relate these differences to variation in quality and fitness. In this study, we fulfilled these tasks in male collared flycatchers (Ficedula albicollis). We characterized the sequential order of syllables with a network analysis approach and studied the consistency of network variables on distinct time scales (within day, between days, and between years), and assessed their relationship with such quality indicators like age, body condition, arrival date, and fitness related proxies like survival to the next year and pairing success. We found that the syllables were associated nonrandomly with one another and both the frequency differences of consecutive syllables and the number of motif types were higher in the original than in randomized syllable sequences. Average degree and small-worldness showed considerable among-individual differences and decreasing repeatability with increasing time scale. Furthermore, we found relationships between male age and average degree among and within individuals. Accordingly, older males produce syllable sequences by using common syllables less often than younger individuals. However, the network variables showed no relationship with fitness-related variables. In conclusion, the sequential organization of birdsong has the potential to encode individual-specific characteristics, which thus could be used as signal in social interactions and thus potentially could be subject to sexual selection.

Experimentally constrained early reproduction shapes life history trajectories and behaviour.

The trade-off between current and future reproduction is a cornerstone of life history theory, but the role of within-individual plasticity on life history decisions and its connections with overall fitness and behaviour remains largely unknown. By manipulating available resources for oviposition at the beginning of the reproductive period, we experimentally constrained individual life history trajectories to take different routes in a laboratory study system, the beetle Callosobruchus maculatus, and investigated its causal effects on fecundity, survival and behaviour. Compared to females without resource limitations, females experiencing restricted conditions for oviposition had reduced fecundity early in life but increased fecundity when resources became plentiful (relative to both the previous phase and the control group) at the expense of longevity. Constrained reproduction in early life also affected behaviour, as movement activity changed differently in the two experimental groups. Experiencing reproductive constraints has, therefore, consequences for future reproduction investments and behaviour, which may lead individuals to follow different life history strategies.

Sex-dependent risk-taking behaviour towards different predatory stimuli in the collared flycatcher.

Prey animals may react differently to predators, which can thus raise plasticity in risk-taking behaviour. We assessed the behavioural responses of nestling-feeding collared flycatcher (Ficedula albicollis) parents towards different avian predator species (Eurasian sparrowhawk, long-eared owl) and a non-threatening songbird (song thrush) by measuring the latency to resume feeding activity. We found that the sexes differed in their responses towards the different stimuli, as males resumed nestling-provisioning sooner after the songbird than after the predator stimuli, while latency of females was not affected by the type of stimulus. Parents breeding later in the season took less risk than early breeders, and mean response also varied across the study years. We detected a considerable repeatability at the within-brood level across stimuli, and a correlation between the latency of parents attending the same nest, implying that they may adjust similarly their risk-taking behaviour to the brood value. Repeated measurements at the same brood suggested that risk-taking behaviour of flycatcher parents is a plastic trait, and sex-specific effects might be the result of sex-specific adjustments of behaviour to the perceived environmental challenge as exerted by different predators. Furthermore, the nest-specific effects highlighted that environmental effects can render consistently similar responses between the parents.

Collision between biological process and statistical analysis revealed by mean centring.

Animal ecologists often collect hierarchically structured data and analyse these with linear mixed-effects models. Specific complications arise when the effect sizes of covariates vary on multiple levels (e.g. within vs. among subjects). Mean centring of covariates within subjects offers a useful approach in such situations, but is not without problems. A statistical model represents a hypothesis about the underlying biological process. Mean centring within clusters assumes that the lower level responses (e.g. within subjects) depend on the deviation from the subject mean (relative) rather than on the absolute scale of the covariate. This may or may not be biologically realistic. We show that mismatch between the nature of the generating (i.e. biological) process and the form of the statistical analysis produce major conceptual and operational challenges for empiricists. We explored the consequences of mismatches by simulating data with three response-generating processes differing in the source of correlation between a covariate and the response. These data were then analysed by three different analysis equations. We asked how robustly different analysis equations estimate key parameters of interest and under which circumstances biases arise. Mismatches between generating and analytical equations created several intractable problems for estimating key parameters. The most widely misestimated parameter was the among-subject variance in response. We found that no single analysis equation was robust in estimating all parameters generated by all equations. Importantly, even when response-generating and analysis equations matched mathematically, bias in some parameters arose when sampling across the range of the covariate was limited. Our results have general implications for how we collect and analyse data. They also remind us more generally that conclusions from statistical analysis of data are conditional on a hypothesis, sometimes implicit, for the process(es) that generated the attributes we measure. We discuss strategies for real data analysis in face of uncertainty about the underlying biological process.

Evolutionary dynamics in the Anthropocene: Life history and intensity of human contact shape antipredator responses.

Humans profoundly impact landscapes, ecosystems, and animal behavior. In many cases, animals living near humans become tolerant of them and reduce antipredator responses. Yet, we still lack an understanding of the underlying evolutionary dynamics behind these shifts in traits that affect animal survival. Here, we used a phylogenetic meta-analysis to determine how the mean and variability in antipredator responses change as a function of the number of generations spent in contact with humans under 3 different contexts: urbanization, captivity, and domestication. We found that any contact with humans leads to a rapid reduction in mean antipredator responses as expected. Notably, the variance among individuals over time observed a short-term increase followed by a gradual decrease, significant for domesticated animals. This implies that intense human contact immediately releases animals from predation pressure and then imposes strong anthropogenic selection on traits. In addition, our results reveal that the loss of antipredator traits due to urbanization is similar to that of domestication but occurs 3 times more slowly. Furthermore, the rapid disappearance of antipredator traits was associated with 2 main life-history traits: foraging guild and whether the species was solitary or gregarious (i.e., group-living). For domesticated animals, this decrease in antipredator behavior was stronger for herbivores than for omnivores or carnivores and for solitary than for gregarious species. By contrast, the decrease in antipredator traits was stronger for gregarious, urbanized species, although this result is based mostly on birds. Our study offers 2 major insights on evolution in the Anthropocene: (1) changes in traits occur rapidly even under unintentional human "interventions" (i.e., urbanization) and (2) there are similarities between the selection pressures exerted by domestication and by urbanization. In all, such changes could affect animal survival in a predator-rich world, but through understanding evolutionary dynamics, we can better predict when and how exposure to humans modify these fitness-related traits.

The link between selection for function and human-directed play behaviour in dogs.

Human-directed play behaviour is a distinct behavioural feature of domestic dogs. But the role that artificial selection for contemporary dog breeds has played for human-directed play behaviour remains elusive. Here, we investigate how human-directed play behaviour has evolved in relation to the selection for different functions, considering processes of shared ancestry and gene flow among the different breeds. We use the American Kennel Club (AKC) breed group categorization to reflect the major functional differences and combine this with observational data on human-directed play behaviour for over 132 breeds across 89 352 individuals from the Swedish Dog Mentality Assessment project. Our analyses demonstrate that ancestor dogs already showed intermediate levels of human-directed play behaviour, levels that are shared with several modern breed types. Herding and Sporting breeds display higher levels of human-directed play behaviour, statistically distinguishable from Non-sporting and Toy breeds. Our results suggest that human-directed play behaviour played a role in the early domestication of dogs and that subsequent artificial selection for function has been important for contemporary variation in a behavioural phenotype mediating the social bond with humans.

The role of common ancestry and gene flow in the evolution of human-directed play behaviour in dogs.

Among-population variance of phenotypic traits is of high relevance for understanding evolutionary mechanisms that operate in relatively short timescales, but various sources of nonindependence, such as common ancestry and gene flow, can hamper the interpretations. In this comparative analysis of 138 dog breeds, we demonstrate how such confounders can independently shape the evolution of a behavioural trait (human-directed play behaviour from the Dog Mentality Assessment project). We combined information on genetic relatedness and haplotype sharing to reflect common ancestry and gene flow, respectively, and entered these into a phylogenetic mixed model to partition the among-breed variance of human-directed play behaviour while also accounting for within-breed variance. We found that 75% of the among-breed variance was explained by overall genetic relatedness among breeds, whereas 15% could be attributed to haplotype sharing that arises from gene flow. Therefore, most of the differences in human-directed play behaviour among breeds have likely been caused by constraints of common ancestry as a likely consequence of past selection regimes. On the other hand, gene flow caused by crosses among breeds has played a minor, but not negligible role. Our study serves as an example of an analytical approach that can be applied to comparative situations where the effects of shared origin and gene flow require quantification and appropriate statistical control in a within-species/among-population framework. Altogether, our results suggest that the evolutionary history of dog breeds has left remarkable signatures on the among-breed variation of a behavioural phenotype.