Puppy whines mediate maternal behavior in domestic dogs.

In mammals, offspring vocalizations typically encode information about identity and body condition, allowing parents to limit alloparenting and adjust care. But how do these vocalizations mediate parental behavior in species faced with the problem of rearing not one, but multiple offspring, such as domestic dogs? Comprehensive acoustic analyses of 4,400 whines recorded from 220 Beagle puppies in 40 litters revealed litter and individual (within litter) differences in call acoustic structure. By then playing resynthesized whines to mothers, we showed that they provided more care to their litters, and were more likely to carry the emitting loudspeaker to the nest, in response to whine variants derived from their own puppies than from strangers. Importantly, care provisioning was attenuated by experimentally moving the fundamental frequency (fo, perceived as pitch) of their own puppies' whines outside their litter-specific range. Within most litters, we found a negative relationship between puppies' whine fo and body weight. Consistent with this, playbacks showed that maternal care was stronger in response to high-pitched whine variants simulating relatively small offspring within their own litter's range compared to lower-pitched variants simulating larger offspring. We thus show that maternal care in a litter-rearing species relies on a dual assessment of offspring identity and condition, largely based on level-specific inter- and intra-litter variation in offspring call fo. This dual encoding system highlights how, even in a long-domesticated species, vocalizations reflect selective pressures to meet species-specific needs. Comparative work should now investigate whether similar communication systems have convergently evolved in other litter-rearing species.

The evolution of sex roles: The importance of ecology and social environment.

Males and females often have different roles in reproduction, although the origin of these differences has remained controversial. Explaining the enigmatic reversed sex roles where males sacrifice their mating potential and provide full parental care is a particularly long-standing challenge in evolutionary biology. While most studies focused on ecological factors as the drivers of sex roles, recent research highlights the significance of social factors such as the adult sex ratio. To disentangle these propositions, here, we investigate the additive and interactive effects of several ecological and social factors on sex role variation using shorebirds (sandpipers, plovers, and allies) as model organisms that provide the full spectrum of sex role variation including some of the best-known examples of sex-role reversal. Our results consistently show that social factors play a prominent role in driving sex roles. Importantly, we show that reversed sex roles are associated with both male-skewed adult sex ratios and high breeding densities. Furthermore, phylogenetic path analyses provide general support for sex ratios driving sex role variations rather than being a consequence of sex roles. Together, these important results open future research directions by showing that different mating opportunities of males and females play a major role in generating the evolutionary diversity of sex roles, mating system, and parental care.

Evolution of acoustic signals associated with cooperative parental behavior in a poison frog.

The emergence of complex social interactions is predicted to be an important selective force in the diversification of communication systems. Parental care presents a key social context in which to study the evolution of novel signals, as care often requires communication and behavioral coordination between parents and is an evolutionary stepping-stone toward increasingly complex social systems. Anuran amphibians (frogs and toads) are a classic model of acoustic communication and the vocal repertoires of many species have been characterized in the contexts of advertisement, courtship, and aggression, yet quantitative descriptions of calls elicited in the context of parental care are lacking. The biparental poison frog, Ranitomeya imitator, exhibits a remarkable parenting behavior in which females, cued by the calls of their male partners, feed tadpoles unfertilized eggs. Here, we characterized and compared calls across three social contexts, for the first time including a parental care context. We found that egg-feeding calls share some properties with both advertisement and courtship calls but also had unique properties. Multivariate analysis revealed high classification success for advertisement and courtship calls but misclassified nearly half of egg feeding calls as either advertisement or courtship calls. Egg feeding and courtship calls both contained less identity information than advertisement calls, as expected for signals used in close-range communication where uncertainty about identity is low and additional signal modalities may be used. Taken together, egg-feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.

Father's care uniquely influences male neurodevelopment.

Mammalian infants depend on parental care for survival, with numerous consequences for their behavioral development. We investigated the epigenetic and neurodevelopmental mechanisms mediating the impact of early biparental care on development of alloparenting behavior, or caring for offspring that are not one's own. We find that receiving high parental care early in life leads to slower epigenetic aging of both sexes and widespread male-specific differential expression of genes related to synaptic transmission and autism in the nucleus accumbens. Examination of parental care composition indicates that high-care fathers promote a male-specific increase in excitatory synapses and increases in pup retrieval behavior as juveniles. Interestingly, females raised by high-care fathers have the opposite behavioral response and display fewer pup retrievals. These results support the concept that neurodevelopmental trajectories are programmed by different features of early-life parental care and reveal that male neurodevelopmental processes are uniquely sensitive to care by fathers.

The Biology and Social Life of Earwigs (Dermaptera).

Earwigs are often known for the forceps-like appendage at the end of their abdomen, urban legends about them crawling into human ears, and their roles as pest and biological control agents. However, they are much less known for their social life. This is surprising, as many of the 1,900 species of earwigs show social behaviors toward eggs, juveniles, and adults. These behaviors typically occur during family and group living, which may be obligatory or facultative, last up to several months, and involve only a few to several hundred related or unrelated individuals. Moreover, many individuals can alternate between solitary and group living during their life cycle, an ability that probably prevailed during the emergence of social life. In this review, I detail the diversity of group living and social behavior in earwigs and show how further developing this knowledge in Dermaptera can improve our general understanding of the early evolution of social life in insects.

Biological Links between Personality and Plasticity: Testing Some Alternative Hypotheses.

AbstractWhen organisms respond behaviorally to a stimulus, they exhibit plasticity, but some individuals respond to the same stimulus consistently differently than others, thereby also exhibiting personality differences. Parent house sparrows express individual differences in how often they feed offspring and how that feeding rate changes with nestling age. Mean feeding rate and its slope with respect to nestling age were positively correlated at median nestling ages but not at hatching, indicating that individuality is primarily in plasticity. Individual differences could arise because of (1) interactions between environmental variables, (2) differences in underlying state or "quality," or (3) differences in the ability to update cues of changing nestling demand. Individual slopes were modestly repeatable across breeding attempts, hinting at the likely action of additional environmental variables, but only brood size was important. I also found few correlates suggesting quality differences. I used short-term brood size manipulations at two nestling ages to test divergent predictions between the three hypotheses. The pattern of correlations between response to the manipulation and individual slope did not fit any single hypothesis. Patterns of sparrow parental care reveal that personality and plasticity are not cleanly separable, and their biology is likely intertwined. New thinking may be needed about the factors parents use in decisions about care and the relevant fitness consequences.

Effects of Parental Care on the Magnitude of Inbreeding Depression: A Meta-Analysis in Fishes.

AbstractInbreeding results from matings between relatives and often leads to a reduction in the fitness of inbred offspring, known as inbreeding depression. There is substantial variation in the magnitude of inbreeding depression among and within species, driven by differences in the biotic and abiotic environment. Recent studies in three species found that parental care has the potential to buffer against inbreeding depression in the offspring, but the generality of this pattern is still unknown. Here, we performed a meta-analysis to test whether variation in the magnitude of inbreeding depression is related to among-species differences in parental care in fishes. We synthesized 536 effect sizes across 56 studies and 18 species, spanning 47 years of research. We found that inbred offspring suffer a smaller reduction in fitness in species that provide biparental care than in species with uniparental or no care. By using a comparative approach, this study provides novel insights into the capacity of parental care to moderate inbreeding depression and suggests that these effects may currently be underappreciated. Considering the potential effects of parental care on inbreeding depression can help us understand why some species avoid inbreeding, whereas others tolerate or even prefer inbreeding, which has important implications for the maintenance of genetic variation within populations.

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.

Extended incubation recesses in sanderlings are impacted by temperature and body condition.

Complex incubation strategies have evolved to solve the trade-off between parent survival and care for their eggs with often brief departures (recesses) that maximize egg survival, and infrequent extended recesses maximizing adult condition. Here we examined incubation behaviour of sanderlings (Calidris alba), a species that exhibits both biparental and uniparental incubation behaviour. During 11 breeding seasons in Greenland, we have quantified incubation variability with thermologgers placed in nests. We estimated the impact of environmental conditions and individual characteristics on the occurrence and the duration of recesses. We found that extended recesses are a unique feature of uniparentals, and their frequency and duration increased in colder temperatures. The relationship was mediated by body condition, with individuals in poor condition performing longer extended recesses in colder temperatures. This suggests that extended recesses may represent a shift towards self-maintenance at the expense of the egg care, allowing birds to continue incubating under unfavourable conditions. Our study illustrates how extended recesses may be a key breeding strategy to overcome high energetic costs associated with incubation. Quantifying such behavioural flexibility paves the way for tracking future behavioural responses of individuals in the face of changing environments.

Evolution of parental care in haploid-diploid plants.

In bryophytes that alternate between haploid gametophytes and diploid sporophytes through sexual reproduction, sporophytes are often attached to and nurtured on the female gametophyte. A similar phenomenon is seen in Florideophyceae (a group of red algae). These systems in which a gametophyte (mother) invests nutrients in sporophytes (offspring) are ideal for studying the evolution of 'parental care' in non-animal organisms. Here, we propose a model of a haploid-diploid life cycle and examine the evolution of maternal investment in sporophytes focusing on two effects: the degree of paternal or maternal control of investment and the number of sporophytes. We find that when the female dominantly controls the investment, the evolutionarily stable level of investment is that which maximizes the expected reproductive success of the female gametophyte. The genomic conflict between maternal and paternal alleles complicates the evolutionary outcome; however, a greater male allelic effect and a higher number of sporophytes favour a higher energy investment, which may lead to evolutionary branching or run-away escalation of the investment level. This suggests that the selfishness of the paternal gene is the evolutionary driver of parental care and that complex structures such as fusion cells in red algae may have evolved to suppress it.

Coevolution of longevity and female germline maintenance.

An often-overlooked aspect of life-history optimization is the allocation of resources to protect the germline and secure safe transmission of genetic information. While failure to do so renders significant fitness consequences in future generations, germline maintenance comes with substantial costs. Thus, germline allocation should trade off with other life-history decisions and be optimized in accordance with an organism's reproductive schedule. Here, we tested this hypothesis by studying germline maintenance in lines of seed beetle, selected for early (E) or late (L) reproduction for 350 and 240 generations, respectively. Female animals provide maintenance and screening of male gametes in their reproductive tract and oocytes. Here, we reveal the ability of young and aged E- and L-females to provide this form of germline maintenance by mating them to males with ejaculates with artificially elevated levels of protein and DNA damage. We find that germline maintenance in E-females peaks at young age and then declines, while the opposite is true for L-females, in accordance with the age of reproduction in the respective regime. These findings identify the central role of allocation to secure germline integrity in life-history evolution and highlight how females can play a crucial role in mitigating the effects of male germline decisions on mutation rate and offspring quality.

Prolactin modulates changes in parental care behaviour in response to perceived paternity in bluegill sunfish (Lepomis macrochirus).

Prolactin is a hormone conserved across all vertebrates and is renowned for its role in reproduction and parental care. Previous studies on prolactin in fish have primarily relied on administration of mammalian prolactin and have suggested that increases in prolactin lead to greater parental care. However, the influence of endogenous prolactin on fish parental care remains unknown. Here, we measure circulating concentrations of endogenous prolactin during parental care in a fish and link these concentrations to parental care behaviour. We provide evidence that male bluegill sunfish with higher circulating concentrations of prolactin provide more parental care to their offspring. Furthermore, we show that nesting males with experimentally reduced perceived paternity have lower circulating prolactin concentrations and perform fewer parental behaviours, facilitating an adaptive investment in offspring in response to paternity cues. Our findings not only confirm the role of endogenous prolactin in modulating parental care behaviour in a fish but also provide a mechanism underlying the adaptive changes in parental care made in response to perceived paternity.

Prolactin is associated with proximity to incubating partner rather than parental care in black-headed gulls.

The peptide hormone prolactin plays an important role in the expression of parental care behaviours across bird and mammal taxa. While a great deal is known about how plasma prolactin concentrations vary across the reproductive cycle, the few studies that investigate how prolactin relates to individual-level variation in parental care have reported mixed results. We argue that, since parental care is also affected by social interactions and environmental constraints, prolactin may better reflect behaviours that are indirectly related to parenting than the absolute level of care that is eventually expressed. In this study, we tested for associations between plasma prolactin and the expression of both parental care and proximity to the partner in incubating black-headed gulls, Chroicocephalus ridibundus. Baseline prolactin levels increased with calendar date but were unrelated to incubation behaviours. However, parents who showed a weaker decrease in prolactin to an acute stressor spent more time in close proximity to their incubating partner while not on the nest themselves, suggesting that individual variation in stress-induced prolactin changes reflect differences in parents' tendency to be closely associated with their partner and the joint nesting attempt. Baseline and stress-induced levels of the stress hormone corticosterone were unrelated to both prolactin levels and parental behaviours, suggesting that this hormone is not a strong moderator of parental care in black-headed gulls. One potential explanation for the link between prolactin dynamics and partner proximity is that prolactin reflects parental motivation to provide parental care or retain contact with the breeding partner, but further work is needed to directly test this hypothesis.

Paternal care plasticity: males care more for early- than late-developing embryos in an arboreal breeding treefrog.

BACKGROUND: Parental care benefits offspring but comes with costs. To optimize the trade-off of costs and benefits, parents should adjust care based on intrinsic and/or extrinsic conditions. The harm to offspring hypothesis suggests that parents should invest more in younger offspring than older offspring because younger offspring are more vulnerable. However, this hypothesis has rarely been comprehensively tested, as many studies only reveal an inverse correlation between parental care and offspring age, without directly testing the effects of offspring age on their vulnerability. To test this hypothesis, we studied Kurixalus eiffingeri, an arboreal treefrog with paternal care. We first performed a field survey by monitoring paternal care during embryonic development. Subsequently, we conducted a field experiment to assess the prevalence of egg predators (a semi-slug, Parmarion martensi) and the plasticity of male care. Finally, we conducted a laboratory experiment to assess how embryo age affects predation by P. martensi. RESULTS: Our results showed that (1) male attendance and brooding frequency affected embryo survival, and (2) males attended and brooded eggs more frequently in the early stage than in the late stage. The experimental results showed that (3) males increased attendance frequency when the predators were present, and (4) the embryonic predation by the semi-slug during the early was significantly higher than in the late stage. CONCLUSIONS: Our findings highlight the importance of paternal care to embryo survival, and the care behavior is plastic. Moreover, our results provide evidence consistent with the predictions of the harm to offspring hypothesis, as males tend to care more for younger offspring which are more vulnerable.

Plumage and eggshell colouration covary with the level of sex-specific parental contributions to nest building in birds.

Interspecific variation in sex-specific contributions to prenatal parental care, including avian nest building, is becoming increasingly better understood as we amass more information on more species. We examined whether sex-specific nest building contributions covary with the colouration of parents and their eggs in 521 species of Western Palearctic birds. Having colourful plumage and laying colourful eggs are costly because of the deposition of pigments in feathers and eggs and/or forming costly nanostructural substrates in feathers, and so it might be expected that those costs covary with the costs of nest building at the level of individuals and/or across species to produce of a suite of codivergent traits. Using a phylogenetically informed approach, we tested the hypothesis that species in which females alone invest energy building nests exhibit less sexual plumage dichromatism. However, we found comparative support for the opposite of this prediction. We then tested that species in which females alone build nests lay more colourful, and costlier, eggs because the dual costs of building nests and laying colourful eggs can only be borne by higher quality individuals. As expected, we found that species in which females build nests alone or together with males are more likely to lay colourfully pigmented eggs relative to species in which only males build nests. Finally, stochastic character mapping provided evidence of the repeated evolution of female-only nest building. Interspecific sex differences in plumage colouration therefore covary in a complex manner with female pre- (nest building) and post-copulatory (egg production) investment in reproduction.

Genome-wide identification and expression analysis of C-type lectins in discus fish (Symphysodon aequifasciatus) during parental care.

Discus fish (Symphysodon aequifasciatus) exhibit a unique parental care behavior: adult discus produces secretion through their skin, on which the larvae live after birth. The immune components in the skin mucus of parental discus would change during different parental care. C-type lectins (CTLs) could identify and eliminate pathogenic microorganisms and play important roles in innate immunity. Studies on CTLs of discus fish especially during parental care, however, are scarce. Here, we identified 186 CTL genes that distributed in 27 linkage groups based on discus genome. Phylogenetic analysis showed that S. aequifasciatus CTL (SaCTL) members were grouped into 14 subfamilies. A total of 80 gene replication events occurred, of which 15 pairs were subjected to segmental duplication and 65 pairs underwent tandem duplication. Ka/Ks ranged from 0.11 (SaCTL25/SaCTL158) to 0.68 (SaCTL36/SaCTL69), all undergoing purifying selection. RNA-seq analysis revealed that SaCTL members, including duplicated genes, in the skin of parental discus show distinct expression patterns in different care stages and between male and female parents. The SaCTL11 was differentially expressed in most care stages and reached the maximum after eggs spawned, but the expression of its paired SaCTL14 was low in each stage. The SaCTL39 increased first and then decreased, reaching a peak in eggs spawned, while paired SaCTL48 first decreased and then increased, reaching a peak in hatched eggs. The SaCTL50 was differentially expressed only in female fish during care, but not in male fish. These results provide new insights into the evolution and potential functional differentiation of CTLs in discus fish during parental care.

Androgen and glucocorticoid profiles throughout extended uniparental paternal care in the eastern hellbender salamander (Cryptobranchus a. alleganiensis).

The behavioral endocrinology associated with reproduction and uniparental male care has been studied in teleosts, but little is known about hormonal correlates of uniparental male care in other ectotherms. To address this gap, we are the first to document the seasonal steroid endocrinology of uniparental male hellbender salamanders during the transition from pre-breeding to nest initiation, and through the subsequent eight months of paternal care. In doing so, we investigated the correlates of nest fate and clutch size, exploring hellbenders' alignment with several endocrinological patterns observed in uniparental male fish. Understanding the endocrinology of hellbender paternal care is also vital from a conservation perspective because high rates of nest failure were recently identified as a factor causing population declines in this imperiled species. We corroborated previous findings demonstrating testosterone and dihydrotestosterone (DHT) to be the primary androgens in hellbender reproduction, and that cortisol circulates as the most abundant glucocorticoid. However, we were unable to identify a prolactin or a "prolactin-like" peptide in circulation prior to or during parental care. We observed âˆ¼ 80 % declines in both primary androgens during the transition from pre-breeding to nest initiation, and again as paternal care progressed past its first month. In the days immediately following nest initiation, testosterone and DHT trended higher in successful individuals, but did not differ with males' clutch size. We did not observe meaningful seasonality in baseline glucocorticoids associated with breeding or nesting. In contrast, stress-induced glucocorticoids were highest at pre-breeding and through the first two months of care, before declining during the latter-most periods of care as larvae approach emergence from the nest. Neither baseline nor stress-induced glucocorticoids varied significantly with either nest fate or clutch size. Both stress-induced cortisol and corticosterone were positively correlated with total length, a proxy for age in adult hellbenders. This is consistent with age-related patterns in some vertebrates, but the first such pattern observed in a wild amphibian population. Generally, we found that nesting hellbenders adhere to some but not all of the endocrinological patterns observed in uniparental male teleosts prior to and during parental care.

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.

Evolutionary change in the construction of the nursery environment when parents are prevented from caring for their young directly.

Parental care can be partitioned into traits that involve direct engagement with offspring and traits that are expressed as an extended phenotype and influence the developmental environment, such as constructing a nursery. Here, we use experimental evolution to test whether parents can evolve modifications in nursery construction when they are experimentally prevented from supplying care directly to offspring. We exposed replicate experimental populations of burying beetles (Nicrophorus vespilloides) to different regimes of posthatching care by allowing larvae to develop in the presence (Full Care) or absence of parents (No Care). After only 13 generations of experimental evolution, we found an adaptive evolutionary increase in the pace at which parents in the No Care populations converted a dead body into a carrion nest for larvae. Cross-fostering experiments further revealed that No Care larvae performed better on a carrion nest prepared by No Care parents than did Full Care larvae. We conclude that parents construct the nursery environment in relation to their effectiveness at supplying care directly, after offspring are born. When direct care is prevented entirely, they evolve to make compensatory adjustments to the nursery in which their young will develop. The rapid evolutionary change observed in our experiments suggests there is considerable standing genetic variation for parental care traits in natural burying beetle populations-for reasons that remain unclear.

Exploring the role of OXTR gene methylation in attachment development: A longitudinal study.

The current study explored longitudinally whether oxytocin receptor gene methylation (OXTRm) changes moderated the association between parental sensitivity changes and children's attachment changes over three waves. Six hundred six Flemish children (10-12 years, 42.8%-44.8% boys) completed attachment measures and provided salivary OXTRm data on seven CpG sites. Their parents reported their sensitive parenting. Results suggest that OXTRm changes hardly link to attachment (in)security changes after the age of 10. Some support was found for interaction effects between parental sensitivity changes and OXTRm changes on attachment changes over time. Effects suggest that for children with increased OXTRm in the promotor region and decreased methylation in the inhibitor region over time, increased parental sensitivity was associated with increased secure attachment and decreased insecure attachment over time.