Sensory pollutants alter bird phenology and fitness across a continent.

Expansion of anthropogenic noise and night lighting across our planet1,2 is of increasing conservation concern3-6. Despite growing knowledge of physiological and behavioural responses to these stimuli from single-species and local-scale studies, whether these pollutants affect fitness is less clear, as is how and why species vary in their sensitivity to these anthropic stressors. Here we leverage a large citizen science dataset paired with high-resolution noise and light data from across the contiguous United States to assess how these stimuli affect reproductive success in 142 bird species. We find responses to both sensory pollutants linked to the functional traits and habitat affiliations of species. For example, overall nest success was negatively correlated with noise among birds in closed environments. Species-specific changes in reproductive timing and hatching success in response to noise exposure were explained by vocalization frequency, nesting location and diet. Additionally, increased light-gathering ability of species' eyes was associated with stronger advancements in reproductive timing in response to light exposure, potentially creating phenological mismatches7. Unexpectedly, better light-gathering ability was linked to reduced clutch failure and increased overall nest success in response to light exposure, raising important questions about how responses to sensory pollutants counteract or exacerbate responses to other aspects of global change, such as climate warming. These findings demonstrate that anthropogenic noise and light can substantially affect breeding bird phenology and fitness, and underscore the need to consider sensory pollutants alongside traditional dimensions of the environment that typically inform biodiversity conservation.

Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians.

The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.

Social parasitism as an alternative reproductive tactic in a cooperatively breeding cuckoo.

Cooperatively nesting birds are vulnerable to social parasites that lay their eggs in host nests but provide no parental care1-4. Most previous research has focused on the co-evolutionary arms race between host defences and the parasites that attempt to circumvent them5-9, but it remains unclear why females sometimes cooperate and sometimes parasitize, and how parasitic tactics arise in cooperative systems10-12. Here we show that cooperative and parasitic reproductive strategies result in approximately equal fitness pay-offs in the greater ani (Crotophaga major), a long-lived tropical cuckoo, using an 11-year dataset and comprehensive genetic data that enable comparisons of the life-histories of individual females. We found that most females in the population nested cooperatively at the beginning of the breeding season; however, of those birds that had their first nests destroyed, a minority subsequently acted as reproductive parasites. The tendency to parasitize was highly repeatable, which indicates individual specialization. Across years, the fitness pay-offs of the two strategies were approximately equal: females who never parasitized (a 'pure cooperative' strategy) laid larger clutches and fledged more young from their own nests than did birds that both nested and parasitized (a 'mixed' strategy). Our results suggest that the success of parasites is constrained by reproductive trade-offs as well as by host defences, and illustrate how cooperative and parasitic tactics can coexist stably in the same population.

Extra Nestlings That Are Condemned to Die Increase Reproductive Success in Hoopoes.

AbstractThe adaptive value of routinely laying more eggs than can be successfully fledged has intrigued evolutionary biologists for decades. Extra eggs could, for instance, be adaptive as insurance against hatching failures. Moreover, because recent literature demonstrates that sibling cannibalism is frequent in the Eurasian hoopoe (Upupa epops), producing extra offspring that may be cannibalized by older siblings might also be adaptive in birds. Here, directed to explore this possibility in hoopoes, we performed a food supplementation experiment during the laying period and a clutch size manipulation during the hatching stage. We found that females with the food supplement laid on average one more egg than control females and that the addition of a close-to-hatch egg at the end of the hatching period increased the intensity of sibling cannibalism and enhanced fledging success in hoopoe nests. Because none of the extra nestlings from the experimental extra eggs survived until fledging, these results strongly suggest that hoopoes obtain fitness advantages by using temporarily abundant resources to produce additional nestlings that will be cannibalized. These results therefore suppose the first experimental demonstration of the nutritive adaptive function of laying extra eggs in vertebrates with parental care.

Maternal Care under Large Clutches with Small Eggs: The Evolution of Life History Traits in Shield Bugs.

AbstractPatterns in the correlated evolution of parental care and life history traits are long established but controversial. Although parental care is related to large egg size in many taxa, conflicting results have also been reported. To test the evolutionary relationships between parental care and life history traits, we performed phylogenetic comparative analyses using shield bugs (Heteroptera: Acanthosomatidae), in which maternal guarding of eggs and young has repeatedly evolved. Our analyses revealed that female body size affected reproductive resource allocation. Contrary to the expectations of current theories, the acquisition of maternal care was associated with small eggs, large clutches, and large egg resource allocation. There was a greater trade-off between egg size and clutch size in caring species than in noncaring species. Egg and hatchling developmental rates were not correlated with egg size but were slower in caring species than in noncaring species. Analyses of evolutionary transitions suggest that the establishment of large clutches, small eggs, and large egg resource allocation preceded the evolution of maternal care. To our knowledge, this is the first study clarifying the evolution of parental care linked with small eggs in invertebrates.

Parenting in a changing environment: A long-term study of prolactin, parental effort and reproductive success in common eiders.

Parental care is regulated by multiple endocrine mechanisms. Among these hormones, prolactin (PRL) is involved in the expression of parental behaviors. Despite the consensus that PRL mediates variation in parental effort with age and body condition, its role in the adjustment of parental effort to fluctuating environmental conditions, including changing predation pressure, still awaits further investigation. To shed light on this knowledge gap, we relied on a long-term monitoring of female common eiders Somateria mollissima (n = 1277 breeding attempts, 2012-2022) incubating under fluctuating predation risk to investigate the link between baseline PRL levels and female minimum age, body condition, clutch size, environmental parameters (predation pressure, climate, nest microhabitat) and hatching success. We predicted that PRL would be higher in older females, those in better condition or incubating larger clutches. We also predicted that females would reduce parental effort when nesting under challenging environmental conditions (high predation pressure or poor climatic conditions), translated into reduced baseline PRL levels. We also explored how variation in PRL levels, female characteristics and environmental parameters were related to hatching success. Following our predictions, PRL levels were positively associated with body condition and female age (before showing a senescent decline in the oldest breeders). However, we did not observe any population-level or individual-level reduction in PRL levels in response to increasing predation pressure. Population-level baseline PRL levels instead increased over the study period, coincident with rising predation threat, but also increasing female body condition and age. While we did not provide evidence for a direct association between baseline PRL levels and predation risk, our results support the idea that elevated baseline PRL levels promote hatching success under internal constraints (in young, inexperienced, breeders or those incubating a large clutch) or constraining environmental conditions (during years of high predation pressure or poor climatic and foraging conditions). Finally, the low repeatability of baseline PRL levels and high interannual variability highlight considerable within-individual flexibility in baseline PRL levels. Further research should explore flexibility in parental effort to changing environmental conditions, focusing on both baseline and stress-induced PRL levels.

A solution to a sex ratio puzzle in Melittobia wasps.

The puzzling sex ratio behavior of Melittobia wasps has long posed one of the greatest questions in the field of sex allocation. Laboratory experiments have found that, in contrast to the predictions of theory and the behavior of numerous other organisms, Melittobia females do not produce fewer female-biased offspring sex ratios when more females lay eggs on a patch. We solve this puzzle by showing that, in nature, females of Melittobia australica have a sophisticated sex ratio behavior, in which their strategy also depends on whether they have dispersed from the patch where they emerged. When females have not dispersed, they lay eggs with close relatives, which keeps local mate competition high even with multiple females, and therefore, they are selected to produce consistently female-biased sex ratios. Laboratory experiments mimic these conditions. In contrast, when females disperse, they interact with nonrelatives, and thus adjust their sex ratio depending on the number of females laying eggs. Consequently, females appear to use dispersal status as an indirect cue of relatedness and whether they should adjust their sex ratio in response to the number of females laying eggs on the patch.

Elucidation of the genetic determination of clutch traits in Chinese local chickens of the Laiwu Black breed.

BACKGROUND: Egg laying rate (LR) is associated with a clutch, which is defined as consecutive days of oviposition. The clutch trait can be used as a selection indicator to improve egg production in poultry breeding. However, little is known about the genetic basis of clutch traits. In this study, our aim was to estimate genetic parameters and identify quantitative trait single nucleotide polymorphisms for clutch traits in 399 purebred Laiwu Black chickens (a native Chinese breed) using a genome-wide association study (GWAS). METHODS: In this work, after estimating the genetic parameters of age at first egg, body weight at first egg, LR, longest clutch until 52 week of age, first week when the longest clutch starts, last week when the longest clutch ends, number of clutches, and longest number of days without egg-laying until 52 week of age, we identified single nucleotide polymorphisms (SNPs) and potential candidate genes associated with clutch traits in Laiwu Black chickens. The restricted maximum likelihood method was used to estimate genetic parameters of clutch pattern in 399 Laiwu Black hens, using the GCTA software. RESULTS: The results showed that SNP-based heritability estimates of clutch traits ranged from 0.06 to 0.59. Genotyping data were obtained from whole genome re-sequencing data. After quality control, a total of 10,810,544 SNPs remained to be analyzed. The GWAS revealed that 421 significant SNPs responsible for clutch traits were scattered on chicken chromosomes 1-14, 17-19, 21-25, 28 and Z. Among the annotated genes, NELL2, SMYD9, SPTLC2, SMYD3 and PLCL1 were the most promising candidates for clutch traits in Laiwu Black chickens. CONCLUSION: The findings of this research provide critical insight into the genetic basis of clutch traits. These results contribute to the identification of candidate genes and variants. Genes and SNPs potentially provide new avenues for further research and would help to establish a framework for new methods of genomic prediction, and increase the accuracy of estimated genetic merit for egg production and clutch traits.

Protective Geometry and Reproductive Anatomy as Candidate Determinants of Clutch Size Variation in Pentatomid Bugs.

AbstractMany animals lay their eggs in clusters. Eggs on the periphery of clusters can be at higher risk of mortality. We asked whether the most commonly occurring clutch sizes in pentatomid bugs could result from geometrical arrangements that maximize the proportion of eggs in the cluster's interior. Although the most common clutch sizes do not correspond with geometric optimality, stink bugs do tend to lay clusters of eggs in shapes that protect increasing proportions of their offspring as clutch sizes increase. We also considered whether ovariole number, an aspect of reproductive anatomy that may be a fixed trait across many pentatomids, could explain observed distributions of clutch sizes. The most common clutch sizes across many species correspond with multiples of ovariole number. However, there are species with the same number of ovarioles that lay clutches of widely varying size, among which multiples of ovariole number are not overrepresented. In pentatomid bugs, reproductive anatomy appears to be more important than egg mass geometry in determining clutch size uniformity. In addition, our analysis demonstrates that groups of animals with little variation in ovariole number may nonetheless lay a broad range of clutch shapes and sizes.

Coloniality and development impact intraclutch consistency of avian eggs: a comparative analysis of the individual repeatability of eggshell size and shape metrics.

In oviparous animals, egg morphology is considered an aspect of the extended phenotype of the laying mother and, thus, can be directly assessed for consistency both within and between individual females. Despite a recently renewed interest in the evolution and mechanics of avian eggshell morphology, we still lack a large-scale, comparative understanding of which egg traits are individually plastic and whether individual consistency is shaped by ecological and life history traits at the species level. Here, we aimed to understand whether intraclutch repeatability per se of different eggshell metrics is an evolving trait that responds to selection pressures from socio-ecological contexts across a diverse group of avian species for which clutch-level eggshell morphology data were available to us. Coloniality, ontogeny, and incubation period had significant impacts on the comparative patterns of relative individual repeatability among two egg metrics (i.e., size and shape), whereas other life history traits (including adult size, clutch size, nest type, migration, breeding latitude, host status of brood parasitism) did not have statistical impacts. Our results also demonstrate that individual consistency has a more widespread phylogenetic distribution than expected by evolutionary contingency across avian diversity. Future analyses should also incorporate the effects of intra- and interspecific covariation in other morphological and physiological traits on the evolution of individual consistency, especially those relevant to egg recognition, including eggshell color and maculation.

Investing in a nest egg: intraspecific variation in the timing of egg laying across a latitudinal gradient.

Avian reproductive strategies vary widely, and many studies of life-history variation have focused on the incubation and hatching stages of nesting. Birds make proximate decisions regarding reproductive investment during the laying stage, and these decisions likely constrain and tradeoff with other traits and subsequent behaviors. However, we know relatively little about egg-laying stage behaviors given the difficulty of locating and monitoring nest sites from the onset of laying. We used non-invasive continuous video recording to quantify variation in the egg-laying behaviors of burrowing owls (Athene cunicularia) along a 1400-km latitudinal gradient in western North America. Burrowing owls laid eggs disproportionately in the morning hours, and that tendency was strongest among first eggs in a clutch. However, selection appeared to act more strongly on laying intervals (the time between laying of consecutive eggs) than on the diel time of laying, and laying intervals varied widely among and within clutches. Laying intervals declined seasonally and with increasing clutch size but increased with increasing burrow temperature and as a function of laying stage nest attentiveness, which may be a strategy to preserve egg viability. Laying interval was positively correlated with the duration of hatching intervals, suggesting that laying interval duration is one mechanism (along with timing of incubation onset) that generates variation in hatching asynchrony. Our results lend support to two general hypotheses to explain laying schedules; selection favors laying eggs in the morning, but other selective pressures may override that pattern. These conclusions indicate that allocation decisions during laying are an important part of avian life-history strategies which are subject to energetic constraints and tradeoffs with other traits.

Ancestral genetic variation in phenotypic plasticity underlies rapid evolutionary changes in resurrected populations of waterfleas.

The role of phenotypic plasticity in adaptive evolution has been debated for decades. This is because the strength of natural selection is dependent on the direction and magnitude of phenotypic responses to environmental signals. Therefore, the connection between plasticity and adaptation will depend on the patterns of plasticity harbored by ancestral populations before a change in the environment. Yet few studies have directly assessed ancestral variation in plasticity and tracked phenotypic changes over time. Here we resurrected historic propagules of Daphnia spanning multiple species and lakes in Wisconsin following the invasion and proliferation of a novel predator (spiny waterflea, Bythotrephes longimanus). This approach revealed extensive genetic variation in predator-induced plasticity in ancestral populations of Daphnia It is unlikely that the standing patterns of plasticity shielded Daphnia from selection to permit long-term coexistence with a novel predator. Instead, this variation in plasticity provided the raw materials for Bythotrephes-mediated selection to drive rapid shifts in Daphnia behavior and life history. Surprisingly, there was little evidence for the evolution of trait plasticity as genetic variation in plasticity was maintained in the face of a novel predator. Such results provide insight into the link between plasticity and adaptation and highlight the importance of quantifying genetic variation in plasticity when evaluating the drivers of evolutionary change in the wild.

Differences in the temporal scale of reproductive investment across the slow-fast continuum in a passerine.

Life-history strategies differ with respect to investment in current versus 'future' reproduction, but when is this future? Under the novel 'temporality in reproductive investment hypothesis', we postulate variation should exist in the time frame over which reproductive costs are paid. Slow-paced individuals should pay reproductive costs over short (e.g. inter-annual) time scales to prevent reproductive costs accumulating, whereas fast-paced individuals should allow costs to accumulate (i.e. senescence). Using Fourier transforms, we quantify adjustments in clutch size with age, across four populations of blue tits (Cyanistes caeruleus). Fast populations had more prevalent and stronger long-term changes in reproductive investment, whereas slower populations had more prevalent short-term adjustments. Inter-annual environmental variation partly accounted for short-, but not long-term changes in reproductive investment. Our study reveals individuals differ in when they pay the cost of reproduction and that failure to partition this variation across different temporal scales and environments could underestimate reproductive trade-offs.

A global meta-analysis reveals higher variation in breeding phenology in urban birds than in their non-urban neighbours.

Cities pose a major ecological challenge for wildlife worldwide. Phenotypic variation, which can result from underlying genetic variation or plasticity, is an important metric to understand eco-evolutionary responses to environmental change. Recent work suggests that urban populations might have higher levels of phenotypic variation than non-urban counterparts. This prediction, however, has never been tested across species nor over a broad geographical range. Here, we conducted a meta-analysis of the avian literature to compare urban versus non-urban means and variation in phenology (i.e. lay date) and reproductive effort (i.e. clutch size, number of fledglings). First, we show that urban populations reproduce earlier and have smaller broods than non-urban conspecifics. Second, we show that urban populations have higher phenotypic variation in laying date than non-urban populations. This result arises from differences between populations within breeding seasons, conceivably due to higher landscape heterogeneity in urban habitats. These findings reveal a novel effect of urbanisation on animal life histories with potential implications for species adaptation to urban environments (which will require further investigation). The higher variation in phenology in birds subjected to urban disturbance could result from plastic responses to a heterogeneous environment, or from higher genetic variation in phenology, possibly linked to higher evolutionary potential.

Tibetan birds lay larger but fewer eggs in a clutch.

How do offspring size and number vary along elevational gradients? This is a striking but rarely addressed question in life-history evolution. Here we comparatively explore it using phylogenetically paired passerine birds of lowland China vs. the Tibetan plateau spanning an elevational range of 18-4500 m. Toward the Tibetan plateau, egg size increased, clutch size decreased and total clutch volume (= clutch size × egg size) did not change, when accounting for major confounding factors. Larger eggs and smaller clutches can be a response to harsh abiotic conditions at higher elevations and the corresponding reduction in food resources required for raising young, respectively. There was a negative correlation between egg size and clutch size after controlling for elevation effect on either trait, suggesting that the trade-off contributed to the expression of these two traits across elevations, given the lack of an elevational trend in total clutch volume. Tibetan birds had a shorter breeding season, prolonged incubation and nestling period than their lowland counterparts. While fewer clutches over the short breeding season may facilitate the increase in egg size, the concentration of annual reproductive investment did not seem to act on clutch size; despite the smaller clutches, hard environments may impose greater costs of parental care on Tibetan birds. The current research provides insight into the evolution of avian life histories across elevations.

Experimentally manipulated food availability affects offspring quality but not quantity in zebra finch meso-populations.

Food availability modulates survival, reproduction and thereby population size. In addition to direct effects, food availability has indirect effects through density of conspecifics and predators. We tested the prediction that food availability in isolation affects reproductive success by experimentally manipulating food availability continuously for 3 years in zebra finches (Taeniopygia guttata) housed in outdoor aviaries. To this end, we applied a technique that mimics natural variation in food availability: increasing the effort required per food reward without affecting diet. Lower food availability resulted in a slight delay of start of laying and fewer clutches per season, but did not affect clutch size or number of offspring reared per annum. However, increasing foraging costs substantially reduced offspring growth. Thus, food availability in isolation did not impact the quantity of offspring reared, at the expense of offspring quality. Growth declined strongly with brood size, and we interpret the lack of response with respect to offspring number as an adaptation to environments with low predictability, at the time of egg laying, of food availability during the period of peak food demand, typically weeks later. Manipulated natal brood size of the parents did not affect reproductive success. Individuals that were more successful reproducers were more likely to survive to the next breeding season, as frequently found in natural populations. We conclude that the causal mechanisms underlying associations between food availability and reproductive success in natural conditions may be more complex than usually assumed. Experiments in semi-natural meso-populations can contribute to further unravelling these mechanisms.

Evolution of sexual cooperation from sexual conflict.

In many species that form pair bonds, males display to their mate after pair formation. These displays elevate the female's investment into the brood. This is a form of cooperation because without the display, female investment is reduced to levels that are suboptimal for both sexes. The presence of such displays is paradoxical as in their absence the male should be able to invest extra resources directly into offspring, to the benefit of both sexes. We consider that the origin of these displays lies in the exploitation of preexisting perceptual biases which increase female investment beyond that which is optimal for her, initially resulting in a sexual conflict. We use a combined population genetic and quantitative genetic model to show how this conflict becomes resolved into sexual cooperation. A cooperative outcome is most likely when perceptual biases are under selection pressures in other contexts (e.g., detection of predators, prey, or conspecifics), but this is not required. Cooperation between pair members can regularly evolve even when this provides no net advantage to the pair and when the display itself reduces a male's contributions to raising the brood. The findings account for many interactions between the sexes that have been difficult to explain in the context of sexual selection.

Nesting Synchrony and Clutch Size in Migratory Birds: Capital versus Income Breeding Determines Responses to Variable Spring Onset.

AbstractSynchronous reproduction of birds has often been explained by benefits from nesting together, but this concept fails to explain observed intraspecific variation and climate-mediated changes of breeding synchrony. Here, we present a theoretical model of birds that store resources for reproduction (capital breeders) to show how breeding synchrony, clutch size, and offspring recruitment respond to changes in timing of first possible breeding date. Our approach is based on individual fitness maximization when both prebreeding foraging and offspring development are time constrained. The model predicts less synchronous breeding, smaller clutch size, and higher chances for offspring recruitment in capital breeding birds that advance their nesting. For contrast, we also show that birds that need to acquire resources during egg laying (income breeders) do not change nesting synchrony but increase clutch size along with earlier breeding. The prediction of stronger nesting synchronization of capital breeders in years with late nesting onset is confirmed by empirical data on breeding synchrony of a high-latitude capital breeding sea duck, the common eider (Somateria mollissima). We predict that in warming high-latitude ecosystems, bird species that depend on stored reserves for reproduction are expected to desynchronize their nesting.

Age Predicts Risky Investment Better Than Residual Reproductive Value.

AbstractLife-history theory predicts that investment in reproduction should increase as future reproductive potential (i.e., residual reproductive value [RRV]) decreases. Researchers have thus intuitively used age as a proxy for RRV and assume that RRV decreases with age when interpreting age-specific investment. Yet age is an imperfect proxy for RRV and may even be a poor correlate in some systems. We used a 31-year study of the nesting ecology of painted turtles (Chrysemys picta) to assess how age and RRV compare in explaining variation in a risky investment behavior. We predicted that RRV would be a better predictor of risky investment than age because RRV accounts for variation in future reproductive potential across life. We found that RRV was high in early life, slowly decreased until midlife, and then steadily decreased to terminal reproduction. However, age predicted risky behavior better than RRV. This finding suggests that stronger correlates of age (e.g., size) may be more responsible for this behavior in turtles. This study highlights that researchers should not assume that age-specific investment is driven by RRV and that future work should quantify RRV to more directly test this key element of life-history theory.

Multilevel Selection on Offspring Size and the Maintenance of Variation.

AbstractMultilevel selection on offspring size occurs when offspring fitness depends on both absolute size (hard selection) and size relative to neighbors (soft selection). We examined multilevel selection on egg size at two biological scales-within clutches and among clutches from different females-using an external fertilizing tube worm. We exposed clutches of eggs to two sperm environments (limiting and saturating) and measured their fertilization success. We then modeled environmental (sperm-dependent) differences in hard and soft selection on individual eggs as well as selection on clutch-level traits (means and variances). Hard and soft selection differed in strength and form depending on sperm availability-hard selection was consistently stabilizing; soft selection was directional and favored eggs relatively larger (sperm limitation) or smaller (sperm saturation) than the clutch mean. At the clutch level, selection on mean egg size was largely concave, while selection on within-clutch variance was weak but generally negative-although some correlational selection occurred between these two traits. Importantly, we found that the optimal clutch mean egg size differed for mothers and offspring, suggesting some antagonism between the levels of selection. We thus identify several pathways that may maintain offspring size variation: environmentally (sperm-) dependent soft selection, antagonistic multilevel selection, and correlational selection on clutch means and variances. Multilevel approaches are powerful but seldom-used tools for studies of offspring size, and we encourage their future use.