Individual Optimization of Reproductive Investment and the Cost of Incubation in a Wild Songbird.

AbstractDespite avid interest in life history trade-offs and the costs of reproduction, evidence that increased parental allocation reduces subsequent breeding productivity is mixed. This uncertainty may be attributable to environmental heterogeneity in space and time, necessitating experiments across a range of ecological contexts. Over three breeding seasons, we cross-fostered clutches between nests to manipulate incubation duration in a wild population of Carolina wrens, a species in which only females incubate, to test for a cost of incubation on current and future reproduction. Prolonged incubation affected maternal productivity in a manner dependent on the current environment and initial investment in eggs, suggesting that incubation is optimized according to other components of reproduction and individual quality. Effects of incubation duration on foster nestling condition varied between years, being costly in one, beneficial in another, and neutral in the third. The proportion of young fledged, females' probability of breeding again within seasons, and subsequent clutch sizes all declined with increasing incubation effort-effects that became more pronounced as seasons progressed. Therefore, costs of incubation were almost entirely dependent on maternal quality and environmental variation, illustrating the importance of conducting experiments across a range of environmental settings for understanding the costs of reproduction and evolution of life histories.

Coming of age in your local mating market: Just a numbers game?

Research Highlight: Woodman, J. P., Cole, E. F., Firth, J. A., Perrins, C. M., & Sheldon, B. C. (2022). Disentangling the causes of age-assortative mating in bird populations with contrasting life-history strategies. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13851. In their study of age-assortative mating, Woodman and colleagues thoroughly and concisely detail its behavioural determinants using datasets, astonishing in themselves, amassed from their decades-long studies of mute swans (Cygnus olor) and great tits (Parus major), species that are respectively longer- and shorter-lived and occupying different segments of the slow/fast life-history continuum. Here, they show that positive age-assortative mating occurs through active, age-based mate selection in mute swans which play the long game, whereas in the shorter-lived great tit this is principally a passive byproduct of demographic processes. That great tits have relatively lower interannual survivorship means that newly recruited, young birds occupy a larger proportion of the breeding population in any given year than occurs in mute swans. The adaptive significance of age-assortative mating is yet to be determined, but the current study provides an exciting possibility for the role of selection on assortative mating generally in either promoting or constraining active mate selection and sexual dimorphism within and across the tree of life.

The effect of climate change on avian offspring production: A global meta-analysis.

Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.

No Evidence of Competition Between the Blacklegged Tick (Acari: Ixodidae) and American Dog Tick on the Rodent Host White-Footed Deermouse (Rodentia: Cricetidae) in Southwestern Tennessee.

Investigations that analyze interspecific associations of vectors on their hosts are important for understanding community structure and implementing ways to comprehend mechanisms of pathogen transmission. We assessed the interspecific association of two tick species (Ixodes scapularis Say (Ixodida: Ixodidae) and Dermacentor variabilis Say (Ixodida: Ixodidae)) on the rodent host Peromyscus leucopus Rafinesque (Rodentia: Cricetidae) at the Hobart Ames Research and Education Center in southwestern Tennessee. Of the rodents captured, 95 (63%) had neither species of tick, 6 (4%) had both tick species, 25 (16%) had I. scapularis only, and 26 (17%) had D. variabilis only. A coefficient of association (C7 = -0.08) was calculated, which suggested there was competition between the two species of ectoparasites, but this value was not significant, indicating that there was a neutral relationship between the tick species on P. leucopus. The co-occurrence of both tick species on their host at the same time suggested that the two tick species can occupy the same host and use the same resources without competing.

Parental favoritism in a wild bird population.

In most taxa with altricial young, offspring solicit food from their parents using a combination of visual and acoustic stimuli, but exactly what these young are communicating, and how selection shapes parental responses, remains unresolved. Theory posits that parents' interpretation and response to begging should vary with the likelihood of a return on their investment. We tested this in a wild population of prothonotary warblers (Protonotaria citrea), predicting that parents bias food non-randomly toward certain individuals within their broods depending on both the size and number of offspring. We observed parent-offspring interactions and detected strong dependence between brood size and nestling size in shaping parental responses to begging. Larger siblings were less likely to solicit food during feeding events than their smaller siblings, but they received a disproportionate share from parents in nests containing fewer-than-average young, whereas the smaller-than-average nestlings were disproportionately fed in broods containing a greater-than-average number of young. These findings suggest that parents respond to begging signals according to multiple social cues, favoring the stronger siblings with greater survival prospects when few copies of their genes are present, but overtly favoring runts to ensure whole-brood survival when capable of fledging more young. Future experimental studies may shed light on the contributions of parental decision-making and memory, how young nestlings learn in parent-offspring communication systems, and the adaptive significance of these behaviors.

Female birds monitor the activity of their mates while brooding nest-bound young.

In addition to food and protection, altricial young in many species are ectothermic and require that endothermic parents provide warmth to foster growth, yet only one parent-typically the female-broods these young to keep them warm. When this occurs, reduced provisioning by males obliges females to forage instead of providing warmth for offspring, favoring the temporal mapping of male activities. We assessed this in a wild house wren population while experimentally feeding nestlings to control offspring satiety. While brooding, females look out from the nest to inspect their surroundings, and we hypothesized that this helps to determine if their mate is nearby and likely to deliver food to the brood (males pass food to brooding females, which pass the food to nestlings). Females looked out from the nest less often when their partner was singing nearby and when his singing and provisioning were temporally linked, signaling his impending food delivery. Females also left to forage less often when their mate was nearby and likely to deliver food. Nestling begging did not affect these behaviors. Females looking out from the nest more often also provisioned at a higher rate and were more likely to divorce and find a new mate prior to nesting again within seasons, as expected if females switch mates when a male fails to meet expectations. Our results suggest anticipatory effects generated by male behavior and that brooding females temporally map male activity to inform decisions about whether to continue brooding or to leave the nest to forage.

Small-mammal characteristics affect tick communities in southwestern Tennessee (USA).

Life histories can influence the degree of parasite infestations on a host. Pressures exerted on hosts based on age and sex convey varying degrees of parasite prevalence due to differences in host lifestyles, but it is not known how interactions between different host traits affect tick numbers. The objective of this study was to determine if host characteristics (e.g., age, sex, weight, and their interactions) affect the mean number of ticks found on small mammals regardless of host species or habitat. Sherman live traps were placed in forest and grass/forb habitats representative of the southeastern United States. After capture, host characteristics were recorded, and hosts were then searched for ticks. A total of 281 small mammals (148 Peromyscus leucopus, 34 P. maniculatus, 76 Sigmodon hispidus, 16 Microtus pinetorum, and 7 Ochrotomys nuttalli) and 610 ticks (488 Dermacentor variabilis, 114 Ixodes scapularis, 1 Amblyomma americanum, and 7 A. maculatum) were collected in this study. Host's age, sex, and weight affected the number of ticks collected from small mammals and significant interaction effects between host traits occurred (weight by sex, weight by age, and sex by age). For instance, female subadult rodents had significantly more ticks compared to female adults, male subadults had significantly fewer ticks compared to male adults, and the number of ticks on a host increased as host body mass increased. These results support the hypothesis that the number of ticks vary on rodent hosts based on life histories and trait interactions. Therefore, understanding the behavioral mechanisms of a host can aid in the management of parasites in the environment.

Posthatching Parental Care and Offspring Growth Vary with Maternal Corticosterone Level in a Wild Bird Population.

Corticosterone is the primary metabolic steroid in birds and is vital for maintaining homeostasis. However, the relationship between baseline corticosterone and reproduction is unclear, and we lack an understanding of how differences in baseline corticosterone at one stage of the breeding cycle influence reproductive effort at later stages. In a wild population of house wrens, we quantified the concentration of corticosterone in yolks of freshly laid eggs as an integrated measure of maternal physiology and related this to a behavioral measure of stress reactivity made during the nestling period, namely, the latency with which females resumed parental activities following a standardized disturbance at their nest (setting up a camera to record provisioning). Females that recently produced eggs containing higher corticosterone concentrations, which were significantly repeatable within females, took longer to resume activity related to parental care (i.e., feeding and brooding young) following the disturbance. Moreover, a female's latency to resume parental activities negatively predicted her provisioning of nestlings with food and the condition of these young at fledging but did not predict the number fledged. We cross-fostered offspring prior to hatching so these effects on maternal behavior are independent of any prenatal maternal effects on nestlings via the egg. These results are consistent with earlier findings, suggesting that females with higher baseline corticosterone during egg laying or early incubation tend to prioritize self-maintenance over reproduction compared with females with lower baseline corticosterone and suggest that a female's latency to return to her nest and resume parental care following a disturbance might represent a simple, functional measure of maternal stress reactivity.

Condition-Dependent Begging Elicits Increased Parental Investment in a Wild Bird Population.

The coevolution of parental supply and offspring demand has long been thought to involve offspring need driving begging and parental care, leaving other hypotheses underexplored. In a population of wild birds, we experimentally tested whether begging serves as a negatively condition-dependent signal of need or a positively condition-dependent signal of quality. Across multiple years, we supplemented nestling house wrens with food shortly after hatching and simultaneously manipulated corticosterone levels to simulate the hunger-induced increase in glucocorticoids thought to mediate begging. This allowed us to also test whether begging is simply a proximate signal of hunger. Days after supplementation ended, food-supplemented nestlings were in better condition than nonsupplemented nestlings and begged for food at an increased rate; their parents, in turn, increased provisioning to a greater extent than parents of nonsupplemented young, as begging positively predicted provisioning. Food-supplemented nestlings therefore attained above-average condition, which predicted their recruitment as breeding adults in the local population. Glucocorticoids increased begging in the short term, but this transient effect depended on satiety. Thus, glucocorticoids promoted begging as a proximate response to hunger, whereas the longer-term changes in nestling condition, begging, and food provisioning suggest that begging ultimately signals offspring quality to elicit increased investment, thereby enhancing offspring survival.

Nest microclimate during incubation affects posthatching development and parental care in wild birds.

It is widely accepted that recent increases in environmental temperature have had a causal effect on changing life histories; however, much of the evidence for this is derived from long-term observations, whereas inferences of causation require experimentation. Here, we assess effects of increased environmental temperature during incubation on posthatching development, nestling begging and parental care, and reproductive success in two wild, cavity-nesting songbirds, the Carolina wren and prothonotary warbler. We heated experimental nests only during incubation, which increased nest-cavity temperature by ca. 1 °C. This reduced the length of the incubation and nestling periods, and reduced fledging success in prothonotary warblers, while nestling Carolina wrens had similar fledging success but reduced body condition in response to increased temperature. Increased nest-cavity temperature during incubation also reduced posthatching begging by nestlings generally and parental care within Carolina wrens specifically, suggesting potential mechanisms generating these carry-over effects. Offspring body mass and fledging age are often predictive of post-fledging survival and recruitment. Thus, our results suggest that increasing temperatures may affect fitness in wild populations in species-specific ways, and induce life-history changes including the classic trade-off parents face between the size and number of offspring.

Line-1: Implications in the etiology of cancer, clinical applications, and pharmacologic targets.

Long interspersed nuclear elements-1 (Line-1 or L1) accounts for approximately 17% of the human genome. The majority of L1s are inactive, but ∼100 remain retrotransposon competent (RC-L1) and able to retrotranspose through RNA intermediates to different locations of the genome. L1 is involved in both disease initiation and progression via retrotransposition dependent and independent mechanisms. Retrotransposed L1 sequences disrupt genetic loci at sites of insertion, while the activities of L1 si/piRNAs, mRNAs, and ORF1 and ORF2 proteins, and have been implicated in the etiology and progression of several human diseases. Despite these relationships, little is known about the clinical utility of L1 as a biomarker of disease initiation and progression, or the utility of small molecules to inhibit and reverse the harmful effects of L1. In this review, we discuss the life cycle of L1, somatic and germline inhibitions, the mechanisms of L1 retrotransposition dependent and independent disease initiation and progression, clinical utilities, and potential of L1s as pharmacologic targets for the treatment of cancer.

Pre- and postnatal effects of experimentally manipulated maternal corticosterone on growth, stress reactivity and survival of nestling house wrens.

Corticosterone plays a central role in maintaining homeostasis, promoting energy acquisition, and regulating the stress response in birds. Exposure to elevated levels of corticosterone during development can profoundly alter offspring behaviour and physiology, but the effects of elevated maternal corticosterone on offspring development remain poorly understood.We tested two competing hypotheses concerning the effect of maternally derived corticosterone on growth and development of free-living house wrens: (i) elevated maternal corticosterone causes damaging effects on nestling phenotype and fitness (collateral damage hypothesis) and (ii) increased maternal corticosterone enhances offspring fitness by preparing nestlings for the environment experienced by their mother (environmental/maternal-matching hypothesis).We used a non-invasive means to increase maternal corticosterone by providing females with corticosterone-injected mealworms prior to and during egg production in the absence of any overt pre-natal maternal stress. To disentangle pre- and post-natal effects of this elevation in maternal corticosterone, we cross-fostered young in two experiments: (i) nestlings of control and experimental females were reared by unmanipulated, natural females in a uniform maternal environment; (ii) a split-brood design that enabled us to assess the interaction between the mother's corticosterone treatment and that of the nestlings.There were significant pre-natal effects of increased maternal corticosterone on nestling growth and survival. Offspring of females experiencing experimentally increased corticosterone were heavier and larger than offspring of control females. There also was a significant interaction between maternal corticosterone treatment and the corticosterone treatment to which young were exposed within the egg in their effect on nestling survival while in the nest; experimental young exhibited greater survival than control young, but only when reared by control mothers. There was also a significant effect of maternal corticosterone treatment on nestling stress reactivity and, in both experiments, on the eventual recruitment of offspring as breeding adults in the local population.These patterns are broadly consistent with the environmental/maternal-matching hypothesis, and highlight the importance of disentangling pre- and post-natal effects of manipulations of maternal hormone levels on offspring phenotype.

Experimental cross-fostering of eggs reveals effects of territory quality on reproductive allocation.

Parental and territory quality are often correlated in territorial birds, and both factors influence the resources allocated to offspring. Surprisingly, the relative contribution of these two components of variation in parental investment remains obscure. We experimentally decoupled the normal covariation between parental quality and territory quality to test the hypothesis that territory quality influences female prenatal and postnatal reproductive allocation. Territories were categorized into low-, intermediate-, and high-quality based on fledging success of nests over the previous 6 years (nesting sites are fixed in space).To decouple covariation between territory quality and individual quality, nestbox entrance size was increased on high-quality territories and left small on poor-quality sites because house wrens (Troglodytes aedon) prefer small over large entrances to their nest sites. We found a significant prenatal effect of territory quality on nestling provisioning: when reared on intermediate-quality territories, nestlings hatching from eggs produced on low-quality territories were provisioned at a higher rate than those hatching from eggs produced on high-quality territories. We propose that the increased provisioning was brought about by increased nestling begging mediated by a maternally derived compound, such as corticosterone, transferred to the eggs of stressed females in poor-quality habitat.

Experimental manipulation of incubation period reveals no apparent costs of incubation in house wrens.

Fitness costs of incubation ensue whenever the trade-off between incubation and foraging leads to suboptimal incubation or decreased parental body condition. We examined the costs of incubation in a wild population of house wrens, Troglodytes aedon, by experimentally extending or decreasing the incubation period by cross-fostering eggs between nests at different stages of incubation (eggs from control nests were cross-fostered at the same stage of incubation). We determined whether parents or offspring bear the costs of incubation by measuring effects on females and offspring within the same breeding season during which the manipulation occurred, but also by evaluating potential trade-offs between current and future reproduction by monitoring return rates of experimental females and recruitment rates of offspring in subsequent breeding seasons. There was no difference in hatching or fledging success across treatments. There was also no effect of incubation duration on female size-corrected mass, and females from different treatments were equally likely to produce a second brood. Nestlings produced by females did not differ in body mass, tarsus length or residual mass. Neither return rates of females, nor the number of offspring recruited, differed across treatments. We conclude, therefore, that although prolonged incubation entails increased energy expenditures, females are able to offset these losses while foraging, thereby mitigating the costs of incubation. This resiliency is more likely to be seen in income breeders, such as house wrens, that retain some ability to recoup energy expended in incubation, than in capital breeders that are constrained by stored energy reserves.

Size of nest-cavity entrance influences male attractiveness and paternal provisioning in house wrens.

In altricial birds, parental provisioning is plastic and can respond to a variety of environmental stimuli. In this study, we manipulated the size of entrances into artificial nest cavities (i.e., nestboxes) in a population of house wrens (Troglodytes aedon) as a means of manipulating a male's sexual attractiveness, and examined changes in parental provisioning. Nest cavities with large entrances are less desirable as nesting sites, and the males at these sites are less attractive to females. Therefore, we predicted that males at boxes that had large entrances would invest more in parental care (i.e., those that succeeded in finding a mate would provision their offspring at a higher rate) than males at nestboxes with small entrances. As predicted, males provisioned their offspring with food at the highest rates at nestboxes with enlarged entrances, and male provisioning effort positively predicted the number of fledglings they produced per egg. Males at these boxes provisioned more than their mates and more than females and males at nestboxes with small entrances. At nestboxes with small entrances, males provisioned at the same rate as females, and female provisioning did not differ significantly between treatments, on average. Male and female provisioning rates were negatively correlated, such that the increase in provisioning by males at nestboxes with enlarged entrances did not enhance nestling condition, likely because food delivery by females declined with increased provisioning by males. However, the amount of time females spent providing warmth for their ectothermic young increased with increases in male provisioning, suggesting that levels of male parental care altered the mode, not necessarily the extent, of care provided by females. These findings suggest that male provisioning is related to sexual attractiveness, and that sexual conflict over biparental care may not be as simple as the assessment of food provisioning might otherwise suggest.

Maternal natal environment and breeding territory predict the condition and sex ratio of offspring.

Females in a variety of taxa adjust offspring sex ratios to prevailing ecological conditions. However, little is known about whether conditions experienced during a female's early ontogeny influence the sex ratio of her offspring. We tested for past and present ecological predictors of offspring sex ratios among known-age females that were produced as offspring and bred as adults in a population of house wrens. The body condition of offspring that a female produced and the proportion of her offspring that were male were negatively correlated with the size of the brood in which she herself was reared. The proportion of sons within broods was negatively correlated with maternal hatching date, and varied positively with the quality of a female's current breeding territory as predicted. However, females producing relatively more sons than daughters were less likely to return to breed in the population the following year. Although correlative, our results suggest that the rearing environment can have enduring effects on later maternal investment and sex allocation. Moreover, the overproduction of sons relative to daughters may increase costs to a female's residual reproductive value, constraining the extent to which sons might be produced in high-quality breeding conditions. Sex allocation in birds remains a contentious subject, largely because effects on offspring sex ratios are small. Our results suggest that offspring sex ratios are shaped by various processes and trade-offs that act throughout the female life history and ultimately reduce the extent of sex-ratio adjustment relative to classic theoretical predictions.

A dynamic threshold model for terminal investment.

Although reproductive strategies can be influenced by a variety of intrinsic and extrinsic factors, life history theory provides a rigorous framework for explaining variation in reproductive effort. The terminal investment hypothesis proposes that a decreased expectation of future reproduction (as might arise from a mortality threat) should precipitate increased investment in current reproduction. Terminal investment has been widely studied, and a variety of intrinsic and extrinsic cues that elicit such a response have been identified across an array of taxa. Although terminal investment is often treated as a static strategy, the level at which a cue of decreased future reproduction is sufficient to trigger increased current reproductive effort (i.e., the terminal investment threshold) may depend on context, including the internal state of the organism or its current external environment, independent of the cue that triggers a shift in reproductive investment. Here, we review empirical studies that address the terminal investment hypothesis, exploring both the intrinsic and extrinsic factors that mediate its expression. Based on these studies, we propose a novel framework within which to view the strategy of terminal investment, incorporating factors that influence an individual's residual reproductive value beyond a terminal investment trigger - the dynamic terminal investment threshold.

Spring temperatures influence selection on breeding date and the potential for phenological mismatch in a migratory bird.

Climate change has affected the seasonal phenology of a variety of taxa, including that of migratory birds and their critical food resources. However, whether climate-induced changes in breeding phenology affect individual fitness, and how these changes might therefore influence selection on breeding date remain unresolved. Here, we use a 36-yr dataset from a long-term, individual-based study of House Wrens (Troglodytes aedon) to test whether the timing of avian breeding seasons is associated with annual changes in temperature, which have increased to a small but significant extent locally since the onset of the study in 1980. Increasing temperature was associated with an advancement of breeding date in the population, as the onset of breeding within years was closely associated with daily spring temperatures. Warmer springs were also associated with a reduced incubation period, but reduced incubation periods were associated with a prolonged duration of nestling provisioning. Nest productivity, in terms of fledgling production, was not associated with temperature, but wetter springs reduced fledging success. Most years were characterized by selection for earlier breeding, but cool and wet years resulted in stabilizing selection on breeding date. Our results indicate that climate change and increasing spring temperatures can affect suites of life-history traits, including selection on breeding date. Increasing temperatures may favor earlier breeding, but the extent to which the phenology of populations might advance may be constrained by reductions in fitness associated with early breeding during cool, wet years. Variability in climatic conditions will, therefore, shape the extent to which seasonal organisms can respond to changes in their environment.

Elevated corticosterone during egg production elicits increased maternal investment and promotes nestling growth in a wild songbird.

Glucocorticoids circulating in breeding birds during egg production accumulate within eggs, and may provide a potent form of maternal effect on offspring phenotype. However, whether these steroids affect offspring development remains unclear. Here, we employed a non-invasive technique that experimentally elevated the maternal transfer of corticosterone to eggs in a wild population of house wrens. Feeding corticosterone-injected mealworms to free-living females prior to and during egg production increased the number of eggs that females produced and increased corticosterone concentrations in egg yolks. This treatment also resulted in an increase in the amount of yolk allocated to eggs. Offspring hatching from these eggs begged for food at a higher rate than control offspring and eventually attained increased prefledging body condition, a trait predictive of their probability of recruitment as breeding adults in the study population. Our results indicate that an increase in maternal glucocorticoids within the physiological range can enhance maternal investment and offspring development.

Within-female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens.

Sex allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within-individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioural polyphenism in females, and its expression varies with seasonal changes in the environment. Between-nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over-represented in the earlier-laid eggs, were in better condition than daughters, which are over-represented in the later-laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within-female changes in offspring sex and not by sex-biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.