When animals are sick, their physiology and behavior change in ways that can impact their offspring. Research is emerging showing that infection risk alone can also modify the physiology and behavior of healthy animals. If physiological responses to environments with high infection risk take place during reproduction, it is possible that they lead to maternal effects. Understanding whether and how high infection risk triggers maternal effects is important to elucidate how the impacts of infectious agents extend beyond infected individuals and how, in this way, they are even stronger evolutionary forces than already considered. Here, to evaluate the effects of infection risk on maternal responses, we exposed healthy female Japanese quail to either an immune-challenged (lipopolysaccharide [LPS] treated) mate or to a healthy (control) mate. We first assessed how females responded behaviorally to these treatments. Exposure to an immune-challenged or control male was immediately followed by exposure to a healthy male, to determine whether treatment affected paternity allocation. We predicted that females paired with immune-challenged males would avoid and show aggression towards those males, and that paternity would be skewed towards the healthy male. After mating, we collected eggs over a 5-day period. As an additional control, we collected eggs from immune-challenged females mated to healthy males. We tested eggs for fertilization status, embryo sex ratio, as well as albumen corticosterone, lysozyme activity, and ovotransferrin, and yolk antioxidant capacity. We predicted that immune-challenged females would show the strongest changes in the egg and embryo metrics, and that females exposed to immune-challenged males would show intermediate responses. Contrary to our predictions, we found no avoidance of immune-challenged males and no differences in terms of paternity allocation. Immune-challenged females laid fewer eggs, with an almost bimodal distribution of sex ratio for embryos. In this group, albumen ovotransferrin was the lowest, and yolk antioxidant capacity decreased over time, while it increased in the other treatments. No differences in albumen lysozyme were found. Both females that were immune-challenged and those exposed to immune-challenged males deposited progressively more corticosterone in their eggs over time, a pattern opposed to that shown by females exposed to control males. Our results suggest that egg-laying Japanese quail may be able to respond to infection risk, but that additional or prolonged sickness symptoms may be needed for more extensive maternal responses.
While infection and perceived infection risk can influence social and reproductive behavior in several taxa, relatively little is known about how infection specifically affects pair bond behaviors. Some pair bond maintenance behaviors may be costly to maintain during infection, and infection could promote avoidance behaviors within an established pair. Many species exhibiting pair bonds are part of larger social groups, and behavioral shifts in established pairs can result in altered extra-pair contact rates that could also shape disease transmission. Using captive zebra finches (Taeniopygia guttata), we examined how an immune challenge with lipopolysaccharide (LPS) influences activity, social behavior, and pair bond maintenance behaviors in established pairs and their healthy neighbors. We observed shifts in individual and pair maintenance behaviors in both immune-challenged pairs and healthy pairs exposed to a social cue of infection (sick conspecifics). Specifically, LPS-challenged birds decreased activity and social interaction attempts relative to control birds, consistent with LPS-induced sickness behavior. LPS-challenged birds also increased the frequency of clumping (perching together in bodily contact) between individuals within a pair. Healthy birds exposed to immune-challenged conspecifics decreased flight activity and increased self-preening, behaviors which could function to limit infection risk. Exploring how both infection and the perceived risk of infection shape behaviors within and among paired individuals will increase our understanding of the role of social behaviors in shaping disease dynamics.
more » « less- NSF-PAR ID:
- 10398567
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Behavioral Ecology
- Volume:
- 34
- Issue:
- 2
- ISSN:
- 1045-2249
- Format(s):
- Medium: X Size: p. 251-260
- Size(s):
- ["p. 251-260"]
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Abstract The neuropeptide oxytocin influences mammalian social bonding by facilitating the building and maintenance of parental, sexual, and same‐sex social relationships. However, we do not know whether the function of the avian homologue mesotocin is evolutionarily conserved across birds. While it does influence avian prosocial behavior, mesotocin's role in avian social bonding remains unclear. Here, we investigated whether mesotocin regulates the formation and maintenance of same‐sex social bonding in pinyon jays (
Gymnorhinus cyanocephalus ), a member of the crow family. We formed squads of four individually housed birds. In the first, “pair‐formation” phase of the experiment, we repeatedly placed pairs of birds from within the squad together in a cage for short periods of time. Prior to entering the cage, we intranasally administered one of three hormone solutions to both members of the pair: mesotocin, oxytocin antagonist, or saline. Pairs received repeated sessions with administration of the same hormone. In the second, “pair‐maintenance” phase of the experiment, all four members of the squad were placed together in a large cage, and no hormones were administered. For both phases, we measured the physical proximity between pairs as our proxy for social bonding. We found that, compared with saline, administering mesotocin or oxytocin antagonist did not result in different proximities in either the pair‐formation or pair‐maintenance phase of the experiment. Therefore, at the dosages and time frames used here, exogenously introduced mesotocin did not influence same‐sex social bond formation or maintenance. Like oxytocin in mammals, mesotocin regulates avian prosocial behavior; however, unlike oxytocin, we do not have evidence that mesotocin regulates social bonds in birds. -
more » « less
Abstract Pair‐bonded primates have uniquely enduring relationships and partners engage in a suite of behaviors to maintain these close bonds. In titi monkeys, pair bond formation has been extensively studied, but changes across relationship tenure remain unstudied. We evaluated differences in behavioral indicators of pair bonding in newly formed (~6 months paired,
n = 9) compared to well‐established pairs (average 3 years paired,n = 8) of titi monkeys (Callicebus cupreus ) as well as sex differences within the pairs. We hypothesized that overall males would contribute more to maintenance than females, but that the pattern of maintenance behaviors would differ between newly formed and well‐established pairs. Each titi monkey (N = 34) participated in a partner preference test (PPT), where the subject was placed in a middle test cage with grated windows separating the subject from the partner on one side and an opposite‐sex stranger on the other side. During this 150‐min behavioral test, we quantified four key behaviors: time in proximity to the partner or stranger as well as aggressive displays toward the partner or stranger. Overall, we found different behavioral profiles representing newly formed and well‐established pair‐bond relationships in titi monkeys and male‐biased relationship maintenance. Males spent ∼40% of their time in the PPT maintaining proximity to the female partner, regardless of relationship tenure. Males from well‐established bonds spent less time (14%) near the female stranger compared to males from newly formed bonds (21%) at the trend level. In contrast, females from well‐established bonds spent less (23%) time near the male partner in the PPT compared to females from newly formed bonds (47%). Aggressive displays were more frequent in newly formed bonds compared to well‐established bonds, especially for females. Scan sampling for homecage affiliation showed that newly formed pairs were more likely to be found tail twining than well‐established pairs. -
null (Ed.)People’s social interactions could influence their risk of developing various diseases, including cancer, according to population-level studies. In particular, studies have identified a so-called widowhood effect where a person’s risk of disease increases following the loss of a spouse. However, the cause of the widowhood effect remains debatable, as it can be difficult to separate the impact of lifestyle changes from biological changes in the individual following bereavement. It is not possible to use laboratory mice to identify a causal biological mechanism, because they do not form long-term relationships with a single partner (pair bonds). However, several species of deer mouse form pair bonds, and suffer from anxiety and stress if these bonds are broken. Naderi et al. used these mice to study the widowhood effect on the risk of developing cancer. First, Naderi et al. grew human lung cancer cells in blood serum taken from mice that were either in a pair bond or had been separated from their partner. The cancer cells grown in the blood of mice with disrupted pair bonds changed size and shape, indicating that these mice were more likely to develop cancer. This effect was not observed when the cells were grown in the blood of bonded deer mice or of another deer mouse species that does not form pair bonds. Naderi et al. also found that the activity of genes involved in the cancer cells’ ability to spread and to stick together was different in pair-bonded mice and in pair-separated mice. Next, Naderi et al. implanted lung cancer cells into the deer mice to study their effects on live animals. When cancer cells from the deer mice were transplanted into laboratory mice with a weakened immune system, the cells taken from pair-bonded deer mice were less likely to grow than the cells from deer mice with disrupted pair bonds. This suggests that the protective effects of pair bonding persist even after removal from the original mouse. These results provide evidence for a biological mechanism of the widowhood effect, where social experiences can alter gene activity relating to cancer growth. In the future, it will be important to determine whether the same applies to humans, and to find out if there are ways to mimic the effects of long-term bonds to improve cancer prognoses.more » « less
-
null (Ed.)The highly controlled migration of neutrophils toward the site of an infection can be altered when they are trained with lipopolysaccharides (LPS), with high dose LPS enhancing neutrophil migratory pattern toward the bacterial derived source signal and super-low dose LPS inducing either migration toward an intermediary signal or dysregulation and oscillatory movement. Empirical studies that use microfluidic chemotaxis-chip devices with two opposing chemoattractants showed differential neutrophil migration after challenge with different LPS doses. The epigenetic alterations responsible for changes in neutrophil migratory behavior are unknown. We developed two mathematical models that evaluate the mechanistic interactions responsible for neutrophil migratory decision-making when exposed to competing chemoattractants and challenged with LPS. The first model, which considers the interactions between the receptor densities of two competing chemoattractants, their kinases, and LPS, displayed bistability between high and low ratios of primary to intermediary chemoattractant receptor densities. In particular, at equilibrium, we observe equal receptor densities for low LPS (< 15ng/mL); and dominance of receptors for the primary chemoattractant for high LPS (> 15ng/mL). The second model, which included additional interactions with an extracellular signal-regulated kinase in both phosphorylated and non-phosphorylated forms, has an additional dynamic outcome, oscillatory dynamics for both receptors, as seen in the data. In particular, it found equal receptor densities in the absence of oscillation for super-low and high LPS challenge (< 0.4 and 1.1 <LPS< 375 ng/mL); equal receptor densities with oscillatory receptor dynamics for super-low LPS (0.5 < LPS< 1.1ng/mL); and dominance of receptors for the primary chemoattractant for super-high LPS (>376 ng/mL). Predicting the mechanisms and the type of external LPS challenge responsible for neutrophils migration toward pro-inflammatory chemoattractants, migration toward pro-tolerant chemoattractants, or oscillatory movement is necessary knowledge in designing interventions against immune diseases, such as sepsis.more » « less
