Heritability and genetic correlations of fear-related behaviour in Red Junglefowl--possible implications for early domestication

Domesticated species differ from their wild ancestors in a number of traits, generally referred to as the domesticated phenotype. Reduced fear of humans is assumed to have been an early prerequisite for the successful domestication of virtually all species. We hypothesized that fear of humans is linked to other domestication related traits. For three generations, we selected Red Junglefowl (ancestors of domestic chickens) solely on the reaction in a standardized Fear of Human-test. In this, the birds were exposed for a gradually approaching human, and their behaviour was continuously scored. This generated three groups of animals, high (H), low (L) and intermediate (I) fearful birds. The birds in each generation were additionally tested in a battery of behaviour tests, measuring aspects of fearfulness, exploration, and sociality. The results demonstrate that the variation in fear response of Red Junglefowl towards humans has a significant genetic component and is genetically correlated to behavioural responses in other contexts, of which some are associated with fearfulness and others with exploration. Hence, selection of Red Junglefowl on low fear for humans can be expected to lead to a correlated change of other behavioural traits over generations. It is therefore likely that domestication may have caused an initial suite of behavioural modifications, even without selection on anything besides tameness.     

Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis

Developmental plasticity of HPA and fear responses in rats has been proposed to be mediated by environment-dependent variation in active maternal care. Here, we review this maternal mediation hypothesis based on the postnatal manipulation literature and on our own recent research in rats. We show that developmental plasticity of HPA and fear responses in rats cannot be explained by a linear single-factor model based on environment-dependent variation in active maternal care. However, by adding environmental stress as a second factor to the model, we were able to explain the variation in HPA and fear responses induced by postnatal manipulations. In this two-factor model, active maternal care and environmental stress (as induced, e.g., by long maternal separations or maternal food restriction) exert independent, yet opposing, effects on HPA reactivity and fearfulness in the offspring. This accounts well for the finding that completely safe and stable, as well as, highly stressful maternal environments result in high HPA reactivity and fearfulness compared to moderately challenging maternal environments. Furthermore, it suggests that the downregulation of the HPA system in response to stressful maternal environments could reflect adaptive developmental plasticity based on the increasing costs of high stress reactivity with increasingly stressful conditions. By contrast, high levels of environmental stress induced by environmental adversity might constrain such adaptive plasticity, resulting in non-adaptive or even pathological outcomes. Alternatively, however, developmental plasticity of HPA and fear responses in rats might be a function of maternal HPA activation (e.g., levels of circulating maternal glucocorticoid hormones). Thus, implying a U-shaped relationship between maternal HPA activation and HPA reactivity and fearfulness in the offspring, increasing maternal HPA activation with increasing environmental adversity would explain the effects of postnatal manipulations equally well. This raises the possibility that variation in active maternal care is an epiphenomenon, rather than a causal factor in developmental plasticity of HPA and fear responses in rats. Developmental plasticity of HPA and fear responses in rats and other animals has important implications for the design of animal experiments and for the well-being of experimental animals, both of which depend on the exact underlying mechanism(s). Importantly, however, more naturalistic approaches are needed to elucidate the adaptive significance of environment-dependent variation of HPA reactivity and fearfulness in view of discriminating between effects reflecting adaptive plasticity, phenotypic mismatch and pathological outcomes, respectively.     

Gregarious nesting in relation to floor eggs in broiler breeders

Gregarious nesting has often been observed in laying hens, where hens prefer to visit a nest already occupied by other hens over empty nests. This may result in overcrowding of the nests which is considered a welfare issue and, moreover, can increase the economic issue of floor eggs. This study aimed to describe gregarious nesting and spatial behavior in broiler breeders and how this relates to genetic background, fearfulness and mating behavior. Five commercially available genetic lines of broiler breeders were housed in 21 pens of 550 females and 50 males (six pens for lines 1 and 2, five pens for line 3 and two pens for lines 4 and 5) during the ages 20–60 weeks. Every 10 weeks, the plumage condition and wounds were assessed of 50 random hens per pen. Avoidance distance and novel object tests were performed to assess fearfulness at four time points. Distribution of eggs over nests was observed for 6 weeks at the onset of egg production at 26 weeks of age, and use of space was recorded at four time points, while (floor) egg production was noted daily per pen. We found differences between genetic lines over time in plumage condition and prevalence of wounds. Fear of humans was highest at the earliest age tested and did not correlate with general fearfulness as assessed by the novel object test. The distribution of eggs over nests was related to genetic background and was more uneven at the earliest age compared to later ages, and a more uneven distribution was correlated with an increased percentage of floor eggs. Distribution of birds over the litter area differed between the genetic lines, and less use of the litter area was correlated with an increased fear of humans and presence of wounds, suggesting an association with aggressive mating behavior. This difference in distribution of the birds could also explain the correlation between increased presence of wounds and decreased percentage of floor eggs. It is concluded that broiler breeders do show gregarious nesting, which is affected by genetic background. Both increased gregarious nesting and wounds are related to increased floor egg percentage, which should be studied further in broiler breeder research. Genetic selection for even use of the available nests and of the litter and slatted area would therefore support both broiler breeder welfare and performance.     

Sexual behaviour in female pigs

This paper reviews the influence of social mechanisms on oestrus and sexual motivation in pigs. The social relations between the animals and the signals they send out can inhibit as well as encourage their social motivation. Social stimuli from both boars and other sows in oestrus tend to induce and synchronise oestrus and ovulation amongst sows. The courting behaviour of boars is also facilitated by social stimuli from other boars. However, when sows are kept under conditions where the social pressure is high, e.g. due to limited space and/or resources, the social stress experienced by particularly the subordinate individuals may inhibit sexual motivation during oestrus. To a large extent this effect seems to be mediated via specific fear reactions towards dominant individuals of sows that have lost many aggressive encounters. For example, fear reduces the sexual motivation during mating and during sexual interactions amongst sows within a group, and fear may thus inhibit their chances of reproductive success. Similarly, fear of humans caused by innate fearfulness or negative handling procedures reduces sexual motivation in the presence of the human handler even when sows are in standing oestrus.     

Fear and exploration in European starlings (Sturnus vulgaris): a comparison of hand-reared and wild-caught birds

The revision of EU legislation will ban the use of wild-caught animals in scientific procedures. This change is partially predicated on the assumption that captive-rearing produces animals with reduced fearfulness. Previously, we have shown that hand-reared starlings (Sturnus vulgaris) indeed exhibit reduced fear of humans compared to wild-caught conspecifics. Here, we asked whether this reduction in fear in hand-reared birds is limited to fear of humans or extends more generally to fear of novel environments and novel objects. Comparing 6-8 month old birds hand-reared in the lab with age-matched birds caught from the wild as fledged juveniles a minimum of 1 month previously, we examined the birds' initial reactions in a novel environment (a small cage) and found that wild-caught starlings were faster to initiate movement compared to the hand-reared birds. We interpret this difference as evidence for greater escape motivation in the wild-caught birds. In contrast, we found no differences between hand-reared and wild-caught birds when tested in novel object tests assumed to measure neophobia and exploratory behaviour. Moreover, we found no correlations between individual bird's responses in the different tests, supporting the idea that these measure different traits (e.g. fear and exploration). In summary, our data show that developmental origin affects one measure of response to novelty in young starlings, indicative of a difference in either fear or coping style in a stressful situation. Our data contribute to a growing literature demonstrating effects of early-life experience on later behaviour in a range of species. However, since we did not find consistent evidence for reduced fearfulness in hand-reared birds, we remain agnostic about the welfare benefits of hand-rearing as a method for sourcing wild birds for behavioural and physiological research.     

Bacteria between protists and phages: from antipredation strategies to the evolution of pathogenicity

Bacteriophages and protists are major causes of bacterial mortality. Genomics suggests that phages evolved well before eukaryotic protists. Bacteria were thus initially only confronted with phage predators. When protists evolved, bacteria were caught between two types of predators. One successful antigrazing strategy of bacteria was the elaboration of toxins that would kill the grazer. The released cell content would feed bystander bacteria. I suggest here that, to fight grazing protists, bacteria teamed up with those phage predators that concluded at least a temporary truce with them in the form of lysogeny. Lysogeny was perhaps initially a resource management strategy of phages that could not maintain infection chains. Subsequently, lysogeny might have evolved into a bacterium-prophage coalition attacking protists, which became a food source for them. When protists evolved into multicellular animals, the lysogenic bacteria tracked their evolving food source. This hypothesis could explain why a frequent scheme of bacterial pathogenicity is the survival in phagocytes, why a significant fraction of bacterial pathogens have prophage-encoded virulence genes, and why some virulence factors of animal pathogens are active against unicellular eukaryotes. Bacterial pathogenicity might thus be one playing option of the stone-scissor-paper game played between phages-bacteria-protists, with humans getting into the crossfire.     

The negative effects of pathogen‐infected prey on predators: a meta‐analysis

Intra‐guild predation (IGP) – where a top predator (IG_Pred) consumes both a basal resource and a competitor for that resource (IG_Prey) – has become a fundamental part of understanding species interactions and community dynamics. IGP communities composed of intraguild predators and prey have been well studied; however, we know less about IGP communities composed of predators, pathogens, and resources. Resource quality plays an important role in community dynamics and may influence IGP dynamics as well. We conducted a meta‐analysis on predator–pathogen–resource communities to determine whether resource quality mediated by the pathogen affected predator life‐history traits and if these effects met the theoretical constraints of IGP communities. To do this, we summarized results from studies that investigated the use of predators and pathogens to control insect pests. In these systems, the predators are the IG_Pred and pathogens are the IG_Prey. We found that consumer longevity, fecundity, and survival decreased by 26%, 31% and 13% respectively, when predators consumed pathogen‐infected prey, making the infected prey a low quality resource. Predators also significantly preferred healthy prey over infected prey. When we divided consumers by enemy type, strict predators (e.g. wolf spiders) had no preference while parasitoids preferred healthy prey. Our results suggest that communities containing parasitoids and pathogens may rarely exhibit intraguild predation; whereas, communities composed of strict predators and pathogens are more likely dominated by IGP dynamics. In these latter communities, the consumption of low and high quality resources suggests that IGP communities composed of strict predators, pathogens and prey should naturally persist, supporting IGP theory. Synthesis We investigated how consuming pathogen‐infected prey influence important life‐history parameters of insect predators. Pathogens are used in a variety of biocontrol programs, especially to control crop pests. We found that true predators (i.e. wolf spiders) have no preference for healthy or infected prey and have reduced fecundity, survival and longevity consuming infected prey. However, parasitoids avoided infected prey when possible. In biocontrol programs with multiple control agents, parasitoids and pathogens would do a better job controlling pests as predators would reduce the amount of pathogen available and have reduced fitness from consuming infected prey. However, theory suggests that true predators, prey and pathogens may coexist long term.     

Personality of hosts and their brood parasites

Brood parasites such as the common cuckoo Cuculus canorus exploit the parental abilities of their hosts, hosts avoid brood parasitism and predation by showing specific behavior such as loss of feathers, emission of fear screams and contact calls, displaying wriggle behavior to avoid hosts or potential prey, pecking at hosts and prey, and expressing tonic immobility (showing behavior like feigning death or rapid escape from predators and brood parasites). These aspects of escape behavior are consistent for individuals but also among sites, seasons, and years. Escape behavior expressed in response to a broad range of cuckoo hosts and prey are consistently used against capture by humans, but also hosts and brood parasites and predators and their prey. An interspecific comparative phylogenetic analysis of escape behavior by hosts and their brood parasites and prey and their predators revealed evidence of consistent behavior when encountering potential parasites or predators. We hypothesize that personality axes such as those ranging from fearfulness to being bold, and from neophobic to curiosity response in brood parasites constitute important components of defense against brood parasitism that reduces the overall risk of parasitism.     

Variation in the strength of inbreeding depression across environments: Effects of stress and density dependence

In what types of environments should we expect to find strong inbreeding depression? Previous studies indicate that inbreeding depression, δ, is positively correlated with the stressfulness of the environment in which it is measured. However, it remains unclear why stress, per se, should increase δ. To our knowledge, only “competitive stress” has a logical connection to δ. Through competition for resources, better quality (outbred) individuals make the environment worse for lower quality (inbred) individuals, accentuating the differences between them. For this reason, we expect inbreeding depression to be stronger in environments where the fitness of individuals is more sensitive to the presence of conspecifics (i.e., where fitness is more density dependent). Indeed, some studies suggest a role for competition within environments, but this idea has not been tested in the context of understanding variation in δ across environments. Using Drosophila melanogaster, we estimated δ for viability in 22 different environments. These environments were simultaneously characterized for (1) stressfulness and (2) density dependence. Although stress and density dependence are moderately correlated with each other, inbreeding depression is much more strongly correlated with density dependence. These results suggest that mean selection across the genome is stronger in environments where competition is intense, rather than in environments that are stressful for other reasons.     

Is domestication driven by reduced fear of humans? Boldness,metabolism and serotonin levels in divergently selected red junglefowl (Gallus gallus)

Domesticated animals tend to develop a coherent set of phenotypic traits. Tameness could be a central underlying factor driving this, and we therefore selected red junglefowl, ancestors of all domestic chickens, for high or low fear of humans during six generations. We measured basal metabolic rate (BMR), feed efficiency, boldness in a novel object (NO) test, corticosterone reactivity and basal serotonin levels (related to fearfulness) in birds from the fifth and sixth generation of the high- and low-fear lines, respectively (44–48 individuals). Corticosterone response to physical restraint did not differ between selection lines. However, BMR was higher in low-fear birds, as was feed efficiency. Low-fear males had higher plasma levels of serotonin and both low-fear males and females were bolder in an NO test. The results show that many aspects of the domesticated phenotype may have developed as correlated responses to reduced fear of humans, an essential trait for successful domestication.     

Tameness correlates with domestication related traits in a Red Junglefowl intercross

Early animal domestication may have been driven by selection on tameness. Selection on only tameness can bring about correlated selection responses in other traits, not intentionally selected upon, which may be one cause of the domesticated phenotype. We predicted that genetically reduced fear towards humans in Red Junglefowl, ancestors of domesticated chickens, would be correlated to other traits included in the domesticated phenotype. Fear level was determined by a standardised behaviour test, where the reaction towards an approaching human was recorded. We first selected birds for eight generations for either high or low fear levels in this test, to create two divergent selection lines. An F3 intercross, with birds from the eighth generation as parentals, was generated to study correlations between fear-of-human scores and other unselected phenotypes, possibly caused by pleiotropy or linkage. Low fear-of-human scores were associated with higher body weight and growth rates, and with increased activity in an open field test, indicating less general fearfulness. In females, low fear-of-human scores were also associated with more efficient fear habituation and in males with an increased tendency to emit food calls in a mirror test, indicating increased social dominance. Low fear-of-human scores were also associated with smaller brain relative to body weight, and with larger cerebrum relative to total brain weight in females. All these effects are in line with the changes observed in domesticated chickens compared to their ancestors, and we conclude that tameness may have been a driving factor underlying some aspects of the domesticated phenotype.     

Generalization of Human Fear Acquisition and Extinction within a Novel Arbitrary Stimulus Category

Adaptive anxiety relies on a balance between the generalization of fear acquisition and fear extinction. Research on fear (extinction) generalization has focused mostly on perceptual similarity, thereby ignoring the importance of conceptual stimulus relations in humans. The present study used a laboratory procedure to create de novo conceptual categories of arbitrary stimuli and investigated fear and extinction generalization among these stimuli. A matching-to-sample task produced two four-member categories of abstract figures. Next, a member from one category was coupled with an aversive electrical stimulation, while a member from the other category was presented alone. As expected, conditioned fear responses generalized to the other members of the first category (skin conductance and online shock-expectancy). Subsequent extinction of the conditioned member also generalized to the other members. However, extinguishing a non-conditioned member failed to reduce fear of the conditioned member itself. We conclude that fears generalize readily across conceptually related stimuli, but that the degree of extinction generalization depends on the stimulus subjected to extinction.     

Secondary osteon size and collagen/lamellar organization (“osteon morphotypes”) are not coupled,but potentially adapt independently for local strain mode or magnitude

In bone, matrix slippage that occurs at cement lines of secondary osteons during loading is an important toughening mechanism. Toughness can also be enhanced by modifications in osteon cross-sectional size (diameter) for specific load environments; for example, smaller osteons in more highly strained “compression” regions vs. larger osteons in less strained “tension” regions. Additional osteon characteristics that enhance toughness are distinctive variations in collagen/lamellar organization (i.e., “osteon morphotypes”). Interactions might exist between osteon diameter and morphotype that represent adaptations for resisting deleterious shear stresses that occur at the cement line. This may be why osteons often have a peripheral ring (or “hoop”) of highly oblique/transverse collagen. We hypothesized that well developed/distinct “hoops” are compensatory adaptations in cases where increased osteon diameter is mechanically advantageous (e.g., larger osteons in “tension” regions would have well developed/distinct “hoops” in order to resist deleterious consequences of co-existing localized shear stresses). We tested this hypothesis by determining if there are correlations between osteon diameters and strongly hooped morphotypes in “tension”, “compression”, and “neutral axis” regions of femora (chimpanzees, humans), radii (horse, sheep) and calcanei (horse, deer). The results reject the hypothesis—larger osteons are not associated with well developed/distinct “hoops”, even in “tension regions” where the effect was expected to be obvious. Although osteon diameter and morphotype are not coupled, osteon diameters seem to be associated with increased strain magnitudes in some cases, but this is inconsistent. By contrast, osteon morphotypes are more strongly correlated with the distribution of tension and compression.     

Susceptibility of Pediococcus isolates to antimicrobial compounds in relation to hop-resistance and beer-spoilage

Background  

Though important in the context of food microbiology and as potential pathogens in immuno-compromised humans, bacterial isolates belonging to the genus Pediococcus are best known for their association with contamination of ethanol fermentation processes (beer, wine, or fuel ethanol). Use of antimicrobial compounds (e.g., hop-compounds, Penicillin) by some industries to combat Pediococcus contaminants is long-standing, yet knowledge about the resistance of pediococci to antimicrobial agents is minimal. Here we examined Pediococcus isolates to determine whether antibiotic resistance is associated with resistance to hops, presence of genes known to correlate with beer spoilage, or with ability to grow in beer.     

Human-induced fear in wildlife: A review

Humans, like natural predators, can induce fear in wildlife, which has the potential to alter species-level survival and fitness. Though anthropogenic impacts on wildlife have been studied in detail, how wildlife respond behaviorally to human presence has been less studied. Here, we provide a literature review on how humans interact with wildlife populations through the ecology of fear framework. Fear responses can be proactive or reactive, and can go beyond behavioral changes to alterations in physiology (such as increases in stress) or alterations in individual chromosome structure. Wildlife are more likely to flee from humans if they possess a larger body size, are female, or have fear-associated genotypes. Intelligence and individual differences lead to variations in wildlife’s fear responses to humans that can make studying fear difficult. Wildlife fear responses to humans depend on environmental factors, including context-specific human presentation and whether the animal was in urban or rural habitats. Human-induced fear in wildlife may have cascading impacts on broader wildlife communities and habitat structure caused by changes in how individual species interact with other species and the environment.     

Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication

Dogs have an unusual ability for reading human communicative gestures (e.g., pointing) in comparison to either nonhuman primates (including chimpanzees) or wolves . Although this unusual communicative ability seems to have evolved during domestication , it is unclear whether this evolution occurred as a result of direct selection for this ability, as previously hypothesized , or as a correlated by-product of selection against fear and aggression toward humans--as is the case with a number of morphological and physiological changes associated with domestication . We show here that fox kits from an experimental population selectively bred over 45 years to approach humans fearlessly and nonaggressively (i.e., experimentally domesticated) are not only as skillful as dog puppies in using human gestures but are also more skilled than fox kits from a second, control population not bred for tame behavior (critically, neither population of foxes was ever bred or tested for their ability to use human gestures) . These results suggest that sociocognitive evolution has occurred in the experimental foxes, and possibly domestic dogs, as a correlated by-product of selection on systems mediating fear and aggression, and it is likely the observed social cognitive evolution did not require direct selection for improved social cognitive ability.     

Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous

Abstract The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables (e.g., temperature and precipitation) and behavioral traits (e.g., boldness, activity level, and aggression) in a clade of spiders that exhibit highly variable social structures (genus Anelosimus). We found that, relative to their subsocial relatives, social species tended to exhibit reduced aggressiveness toward prey, increased fearfulness toward predators, and reduced activity levels, and they tended to occur in warm, wet habitats with low average wind velocities. Within-species variation in aggressiveness and boldness was also positively associated with sociality. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four test species (Anelosimus eximius, Anelosimus rupununi, Anelosimus guacamayos, and Anelosimus oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance. In all four test species, we found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups. Mixed groups were more effective at subduing medium and large prey, and mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects.     

Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey

The mere presence of predators (i.e., predation risk) can alter consumer physiology by restricting food intake and inducing stress, which can ultimately affect prey‐mediated ecosystem processes such as nutrient cycling. However, many environmental factors, including conspecific density, can mediate the perception of risk by prey. Prey conspecific density has been defined as a fundamental feature that modulates perceived risk. In this study, we tested the effects of predation risk on prey nutrient stoichiometry (body and excretion). Using a constant predation risk, we also tested the effects of varying conspecific densities on prey responses to predation risk. To answer these questions, we conducted a mesocosm experiment using caged predators (Belostoma sp.), and small bullfrog tadpoles (Lithobates catesbeianus) as prey. We found that L. catesbeianus tadpoles adjust their body nutrient stoichiometry in response to predation risk, which is affected by conspecific density. We also found that the prey exhibited strong morphological responses to predation risk (i.e., an increase in tail muscle mass), which were positively correlated to body nitrogen content. Thus, we pose the notion that in risky situations, adaptive phenotypic responses rather than behavioral ones might partially explain why prey might have a higher nitrogen content under predation risk. In addition, the interactive roles of conspecific density and predation risk, which might result in reduced perceived risk and physiological restrictions in prey, also affected how prey stoichiometry responded to the fear of predation.     

Prey availability influences habitat tolerance: an explanation for the rarity of peregrine falcons in the tropics

The density and productivity of peregrine falcon Falco peregri nus populations correlate positively with distance from the Equator, while habitat specificity increases with proximity to the Equator. Low peregrine densities in the tropics may he a result of competition with similar conveners (e.g. the lanner falcon F. biarmicus in Africa), which replace them in many areas. Alternatively, tropical peregrines may he limited by resource deficiencies that do not affect their close relatives. Data from peregrine and lanner populations in South Africa support the resource deficiency hypothesis, and there is no evidence to suggest direct competition between the two species. In areas where prey are not spatially or temporally concentrated, or otherwise particularly vulnerable to attack, morphological and behavioural specializations of peregrines probably restrict them to optimal foraging conditions. The relative dynamics of.Arctic and temperate vs tropical prey populations is suggested as an important factor determining peregrine distribution globally. Populations of other widespread hut particularly specialized avian predators (e.g. osprey Pandion haliaetus) may he similarly controlled. Food limitation (in terms of a dearth of particularly vulnerable prey) in the tropics has resulted in specialization and rarity in peregrines and generalization and relative abundance in similar congeners.     

The interaction between island geomorphology and environmental parameters drives Adélie penguin breeding phenology on neighboring islands near Palmer Station,Antarctica

Despite many studies on Adélie penguin breeding phenology, understanding the drivers of clutch initiation dates (CIDs, egg 1 lay date) is limited or lacks consensus. Here, we investigated Adélie penguin CIDs over 25 years (1991–2016) on two neighboring islands, Torgersen and Humble (<1 km apart), in a rapidly warming region near Palmer Station, Antarctica. We found that sea ice was the primary large‐scale driver of CIDs and precipitation was a secondary small‐scale driver that fine‐tunes CID to island‐specific nesting habitat geomorphology. In general, CIDs were earlier (later) when the spring sea ice retreat was earlier (later) and when the preceding annual ice season was shorter (longer). Island‐specific effects related to precipitation and island geomorphology caused greater snow accumulation and delayed CIDs by ~2 days on Torgersen compared to Humble Island. When CIDs on the islands were similar, conditions were mild with less snow across breeding sites. At Torgersen Island, the negative relationship between CID and breeding success highlights detrimental effects of delayed breeding and/or snow on penguin fitness. Past phenological studies reported a relationship between air temperature and CID, assumed to be related to precipitation, but we found air temperature was more highly correlated to sea ice, revealing a misinterpretation of temperature effects. Finally, contrasting trends in CIDs based on temporal shifts in regional sea ice patterns revealed trends toward earlier CIDs (4–6 day advance) from 1979 to 2009 as the annual ice season shortened, and later CIDs (7–10 day delay) from 2010 to 2016 as the annual ice season lengthened. Adélie penguins tracked environmental conditions with flexible breeding phenology, but their life history remains vulnerable to subpolar weather conditions that can delay CIDs and decrease breeding success, especially on landscapes where geomorphology facilitates snow accumulation.