Sex-specific influence of communal breeding experience on parenting performance and fitness in a burying beetle

Communal breeding, wherein multiple conspecifics live and reproduce together, may generate short-term benefits in terms of defence and reproduction. However, its carry-over effects remain unclear. We experimentally tested the effects of communal breeding on parental care and reproduction in burying beetles (Nicrophorus vespilloides), which use carcasses as breeding resources and provide parental care to offspring. We subjected individuals to communal or non-communal breeding (i.e. pair breeding) during their first breeding event and to non-communal breeding during their second breeding event. We measured the parental care of individuals and of groups and the reproductive success of groups during both breeding events. In communal groups, large individuals became dominant and largely monopolized the carcass, whereas small individuals (i.e. subordinates) had restricted access to the carcass. At the first breeding event, large males in communal groups spent more time providing care than large males in non-communal groups, whereas such an effect was not observed for large females and small individuals. Reproductive successes were similar in communal and non-communal groups, indicating no short-term benefits of communal breeding in terms of reproduction. Compared with males from non-communal groups, males originating from communal groups produced a larger size of brood during their second breeding event, whereas such an effect was not observed for females. Our results demonstrate the sex-specific effects of communal breeding experience on parenting performance and fitness

Parental Care System and Brood Size Drive Sex Difference in Reproductive Allocation:An Experimental Study on Burying Beetles

Life-history theory predicts that increased resource allocation in current reproduction comes at the cost of survival and future reproductive fitness. In taxa with biparental care, each parent can adjust investment on current reproduction according to changes in their partner’s effort, but these adjustments may be different for males and females as they may have different reproductive strategies. Numerous theoretical and empirical studies have proposed the mechanism underlying such adjustments. In addition, the value of the brood or litter (brood size) has also been suggested to affect the amount of care through manipulation of brood size. While the two conditions have been studied independently, the impact of their interplay on potential sex-dependent future reproductive performance remains largely unknown. In this study, we simultaneously manipulated both care system (removal of either parent vs. no removal) and brood size in a burying beetle (Nicrophorus vespilloides) to understand their joint effect on reproductive allocation and trade-off between current and future reproduction. Our results show that males compensated for mate loss by significantly increasing the level of care regardless of brood size, while females exhibited such compensation only for small brood size. Additionally, with an increase in allocation to current reproduction, males showed decreased parental investment during the subsequent breeding event as a pair. These findings imply a dual influence of parental care system and brood size on allocation in current reproduction. Moreover, the impact of such adjustments on sex-dependent differences in future reproduction (parental care, larvae number, and average larval mass at dispersal) is also demonstrated. Our findings enhance the understanding of sex roles in parental investment and highlight their importance as drivers of reproductive allocation

Males and females of a polygamous songbird respond differently to mating opportunities

Parents are expected to make fine-tuned decisions by weighing the benefits of providing care to increase offspring survival against that of deserting to pursue future mating opportunities. A higher incentive for the rarer sex in the population indicates an impact of mating opportunities on parental care decisions. However, in a dynamic breeding system, deserting the offspring and searching for a new mate would influence mating opportunities for both sexes. Sex-specific costs and benefits are expected to influence males’ and females’ parenting strategies in different ways. Here, we investigated Chinese penduline tits, Remiz consobrinus, which exhibit flexible parental care strategies: uniparental care by the male or female, biparental care, and biparental desertion occur in the same population. We show that male penduline tits change their parental behavior over the breeding season; they desert clutches produced early in the season but care for the late season clutches. The change in male parenting behavior is consistent with the seasonal decline in mating opportunities. In contrast, parenting by females did not change over the breeding season, nor was it associated with seasonal variation in mate availability. Taken together, mating opportunities have different associations with parental behavior of male and female Chinese penduline tits. We recommend an inclusion of mating opportunities for both sexes simultaneously in order to understand one of the fundamental decisions in parental care evolution—care or desert

Effects of early-life conditions on innate immune function in adult zebra finches

Early life conditions can affect individuals for life, with harsh developmental conditions resulting in lower fitness, but the underlying mechanisms are not well understood. We hypothesized that immune function may be part of the underlying mechanism, when harsh developmental conditions result in less effective immune function. We tested this hypothesis by comparing innate immune function between zebra finches (Taeniopygia guttata) in adulthood (n=230; age 108–749 days) that were reared in either small or large broods. We used this experimental background to follow up our earlier finding that finches reared in large broods have a shorter lifespan. To render a broad overview of innate immune function, we used an array of six measures: bacterial killing capacity, hemagglutination, hemolysis, haptoglobin, nitric oxide and ovotransferrin. We found no convincing evidence for effects of natal brood size on any of the six measures of innate immune function. This raised the question whether the origin of variation in immune function was genetic, and we therefore estimated heritabilities using animal models. However, we found heritability estimates to be low (range 0.04–0.11) for all measured immune variables, suggesting variation in innate immune function can largely be attributed to environmental effects independent of early-life conditions as modified by natal brood size

Seasonal differences in baseline innate immune function are better explained by environment than annual cycle stage in a year-round breeding tropical songbird

C.J.N. was supported by a studentship funded by the Leventis Conservation Foundation through the University of St. Andrews UK and an Ubbo Emmius grant of the University of Groningen, The Netherlands. B.I.T. was supported by the Netherlands Organisation for Scientific Research (NWO-Vidi 864.10.012).1. Seasonal variation in innate immunity is often attributed to either temporal environmental variation or to life history trade-offs that arise from specific annual cycle stages but decoupling them is difficult in natural populations. 2.  Here, we effectively decouple seasonal environmental variation from annual cycle stage effects by exploiting cross-seasonal breeding and moult in the tropical Common Bulbul Pycnonotus barbatus. We test how annual cycle stage interacts with a key seasonal environmental variable, rainfall, to determine immunity at population and individual level. If immune challenge varies with precipitation, we might expect immune function to be higher in the wet season due to increased environmental productivity. If breeding or moult imposes resource constraints on birds, depending on or independent of precipitation, we might expect lower immune indices during breeding or moult. 3.  We sampled blood from 818 birds in four annual cycle stage categories: breeding, moult, simultaneous breeding and moulting, or neither. We quantified indices of innate immunity (haptoglobin, nitric oxide (NOx) and ovotransferrin concentrations, and haemagglutination and haemolysis titres) over two annual cycles of wet and dry seasons. 4.  Environment (but not annual cycle stage or interactions between both) explained variation in all immune indices, except NOx. NOx concentration differed between annual cycle stages but not between seasons. However, within the wet season, haptoglobin, NOx, ovotransferrin and haemolysis differed significantly between breeding and non-breeding females. Aside from some recorded inconsistences, population level results were largely similar to results within individuals that were measured repeatedly. Unexpectedly, most immune indices were higher in the dry season and during breeding. 5.  Higher immune indices may be explained if fewer or poorer quality resources force birds to increase social contact, thereby exposing individuals to novel antigens and increased infection risk, independently of environmental productivity. Breeding birds may also show higher immunity if less immune-competent and/or infected females omit breeding. We conclude that seasonal environmental variation impacts immunity more directly in natural animal populations than via resource trade-offs. In addition, immune indices were more often variable within than among individuals, but some indices are characteristic of individuals, and so may offer selective advantages if heritable.Publisher PDFPeer reviewe

Effects of manipulated food availability and seasonality on innate immune function in a passerine

The innate immune system is essential for survival, yet many immune traits are highly variable between and within individuals. In recent years, attention has shifted to the role of environmental factors in modulating this variation. A key environmental factor is food availability, which plays a major role in shaping life histories, and may affect resource allocation to immune function through its effect on nutritional state. We developed a technique to permanently increase foraging costs in seed-eating birds, and leveraged this technique to study the effects of food availability on the innate immune system over a 3-year period in 230 zebra finches housed in outdoor aviaries. The immune components we studied were haptoglobin, ovotransferrin, nitric oxide, natural antibodies through agglutination, complement-mediated lysis, and killing capacity of Escherichia coli and Candida albicans, covering a broad spectrum of the innate immune system. We explored the effects of food availability in conjunction with other potentially important variables: season, age, sex and manipulated natal brood size. Increased foraging costs affected multiple components of the immune system, albeit in a variable way. Nitric oxide and agglutination levels were lower under harsh foraging conditions, while Escherichia coli killing capacity was increased. Agglutination levels also varied seasonally, but only at low foraging costs. C. albicans killing capacity was lower in winter, and even more so for animals in harsh foraging conditions that were raised in large broods. Effects of food availability on ovotransferrin were also seasonal, and only apparent in males. Haptoglobin levels were independent of foraging costs and season. Males had higher levels of immune function than females for three of the measured immune traits. Innate immune function was independent of age and manipulated natal brood size. Our finding that food availability affects innate immune function suggests that fitness effects of food availability may at least partially be mediated by effects on the immune system. However, food availability effects on innate immunity varied in direction between traits, illustrating the complexity of the immune system and precluding conclusions on the level of disease resistance

No evidence for parasitism-linked changes in immune function or oxidative physiology over the annual cycle of an avian species

Temporally changing environmental conditions occur in most parts of the world and can exert strong pressure on the immune defense of organisms. Seasonality may result in changes in physiological traits over the year, and such changes may be essential for the optimization of defense against infections. Evidence from field and laboratory studies suggest the existence of links between environmental conditions, such as infection risk, and the ability of animals to mount an immune response or to overcome infections; however, the importance of parasites in mediating seasonal change in immune defense is still debated. In this study, we test the hypothesis that seasonal change in immune function and connected physiological traits is related to parasite infection. We sampled captive house sparrows (Passer domesticus) once every 2 mo over 14 mo and compared the annual variation in 12 measures of condition, immune function, antioxidant status, and oxidative damage among birds naturally infested with coccidians or medicated against these parasites. We found significant variation in 10 of 12 traits over the year. However, we found little support for parasite-mediated change in immune function and oxidative status in captive house sparrows. Of the 12 measures, only one was slightly affected by parasite treatment. In support of the absence of any effect of coccidians on the annual profile of the condition and physiological traits, we found no consistent relationships between the intensity of infestation and these response variables over the year. Our results show that chronic coccidian infections have limited effect on the seasonal changing of physiological traits and that the patterns of these measures are probably more affected by acute infection and/or virulent parasite strains

Constitutive innate immunity of tropical House Wrens varies with season and reproductive activity

In lowland Neotropical regions, where air temperature and day length remain relatively constant year round, seasonality is determined primarily by changes in rainfall. The wet season triggers the start of breeding for many Neotropical birds but also alters the antigenic environment, likely increasing the risk of disease transmission. We explored 2 hypotheses about temporal variation in constitutive innate immunity of a Neotropical bird, the House Wren (Troglodytes aedon). The antigen response hypothesis proposes that Neotropical wrens upregulate their immune function in the wet season either in anticipation of or in response to vectors that become more prevalent. The resource constraint hypothesis proposes that during periods of putative high resource demand, such as when parents are feeding young, immune function should be compromised and downregulated. Controlling for reproductive stage, we found that microbicidal capacity of blood against Escherichia coli was higher in the wet than the dry season, consistent with the antigen response hypothesis. Phagocytosis of E. coli and Staphylococcus aureus did not differ between wet and dry seasons. Microbicidal capacity and H/L ratio of tropical House Wrens did not vary among reproductive stages, and our data offered no support for the idea that immune function is compromised during the period when parents are feeding young

Seasonal Patterns and Relationships among Coccidian Infestations, Measures of Oxidative Physiology, and Immune Function in Free-Living House Sparrows over an Annual Cycle

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Shifts in bacterial communities of eggshells and antimicrobial activities in eggs during incubation in a ground-nesting passerine

Microbial invasion of egg contents is a cause of embryonic death. To counter infection risks, the embryo is protected physically by the eggshell and chemically by antimicrobial proteins. If microbial pressure drives embryo mortality, then females may have evolved, through natural selection, to adapt their immune investment into eggs. Although frequently hypothesized, this match between immune allocation and microorganisms has not been explored yet. To examine if correlations between microbes on eggs and immunity in eggs exist, we collected eggs from red-capped larks (Calandrella cinerea) and simultaneously examined their bacterial communities and antimicrobial components--pH, lysozyme and ovotransferrin--during natural incubation. Using molecular techniques, we find that bacterial communities are highly dynamic: bacterial abundance increases from the onset to late incubation, Shannon's α-diversity index increases during early incubation stages, and β-diversity analysis shows that communities from 1 day-old clutches are phylogenetically more similar to each other than the older ones. Regarding the antimicrobials, we notice a decrease of pH and lysozyme concentration, while ovotransferrin concentration increases during incubation. Interestingly, we show that two eggs of the same clutch share equivalent immune protection, independent of clutch age. Lastly, our results provide limited evidence of significant correlation between antimicrobial compounds and bacterial communities. Our study examined simultaneously, for the first time in a wild bird, the dynamics of bacterial communities present on eggshells and of albumen-associated antimicrobial components during incubation and investigated their relationship. However, the link between microorganisms and immunity of eggs remains to be elucidated further. Identifying invading microbes and their roles in embryo mortality, as well as understanding the role of the eggshell microbiome, might be key to better understand avian strategies of immune maternal investment