Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse

Maternal behaviour has profound, long-lasting implications for the health and well-being of developing offspring. In the monogamous California mouse (Peromyscus californicus), care by both parents is critical for offspring survival. We tested the hypothesis that similar to maternal care in rodents, paternal huddling and grooming (HG) behaviour can be transmitted to future generations via behavioural mechanisms. In California mice, testosterone maintains paternal HG behaviour. In the present study, we randomly assigned a group of male California mice to castration or sham-operated conditions and allowed them to raise their offspring normally. Adult sons of these males were paired with a female, and they were observed interacting with their own offspring. We found that like their fathers, the sons of castrated males huddled and groomed their young at lower levels than the sons of sham-operated fathers. The sons of castrates also retrieved pups more frequently. When both parents were present, the sons of castrates also showed a trend towards engaging in less exploratory behaviour. These data support the hypothesis that paternal behaviour, like maternal behaviour, can be transferred to future generations via epigenetic mechanisms and suggest that in a biparental species both parents contribute to offspring behavioural development.     

Spatial structure and parental aggression in eider broods

The spatial position of young animals within a brood affects their survival, so that marginal individuals are at greater risk of predation. Spatial brood structuring may be caused by differences in offspring size, age, hunger, or active parental manipulation through aggression. Nepotistic manipulation of brood structure would confer fitness benefits for parents accepting nondescendant young. However, insufficient kin recognition has often been considered to preclude such nepotism in birds, particularly in precocial waterfowl. We explored the spatial structure of ducklings within broods of eiders, Somateria mollissima, a seaduck with frequent brood amalgamation. We compared the distribution of ducklings of different origin relative to reference females whose kinship to the ducklings was known. We also observed female aggression towards ducklings, to evaluate the role of parental manipulation of brood structure. We found a nonrandom distribution of ducklings within broods; a female's own young were on average closer to her than unrelated young were. We also found evidence for parental nepotism: whether the brood contained unrelated young was the strongest predictor of female aggression towards ducklings. The spatial position, hatch weight and relative size of ducklings showed no significant correlations with each other, suggesting that active parental manipulation may be needed to explain the observed spatial structure. Our study conflicts with previous anecdotal evidence suggesting that brood amalgamation in eiders results in the disintegration of parent-offspring bonds, preventing parental exploitation of nondescendant young. It also opens up the possibility that the spatial position of ducklings depends on their mother's status in the female dominance hierarchy. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Dispersal distance is influenced by parental and grand-parental density

Non-genetic transmission of information across generations, so-called parental effects, can have significant impacts on offspring morphology, physiology, behaviour and life-history traits. In previous experimental work using the two-spotted spider mite Tetranychus urticae Koch, we demonstrated that dispersal distances increase with local density and levels of genetic relatedness. We here show that manipulation of parental and grand-parental density has a significant effect on offspring dispersal distance, of the same order of magnitude as manipulation of offspring density. We demonstrate that offspring exposed to the same density disperse further if they were born to parents exposed to higher density compared with parents exposed to low density. Offspring dispersal distance also increases when grand-parents were exposed to higher density, except for offspring exposed to low densities, which disperse at shorter distances whatever the grand-parental density. We also show that offspring from mothers exposed to higher densities were overall larger, which suggests that parents in high densities invest more in individual offspring, enabling them to disperse further. We propose that our findings should be included in models investigating the spread rate of invasive species or when predicting the success of conservation measures of species attempting to track changing climates.     

Maternal testosterone influences a begging component that makes fathers work harder in chick provisioning

In species with biparental care, parents disagree evolutionarily over the amount of care that each of them is willing to provide to offspring. It has recently been hypothesised that females may try to manipulate their mates by modifying offspring begging behaviour through yolk hormone deposition, shifting the division of labour in their own favour. To test this hypothesis we first investigated how yellow-legged gull (Larus michaellis) parents feed offspring in relation to each component of complex begging behaviour and if feeding behaviour varies between sexes. Then we investigated the effect of yolk testosterone on chicks' begging by experimentally increasing yolk testosterone levels. Our results revealed that yolk testosterone has a component-specific effect on chicks' begging, specifically increasing the number of chatter calls. Parental feeding effort was influenced by the number of chatter calls emitted by chicks, but most importantly, the influence was stronger in male than in female parents. Moreover, chick body mass increased with the number of paternal feeds. In conclusion, these results show that female gulls may use yolk testosterone deposition to exploit their partners as predicted by the ‘Manipulating Androgen Hypothesis (MAH)’.     

Cooperation, conflict, and crèching behavior in goldeneye ducks

Crèching behavior, or brood amalgamation, results in offspring being reared by adults other than their genetic parents. Although a variety of hypotheses have been proposed to explain this behavior, most assume either that brood amalgamation is accidental (i.e., nonselected) or that adoption of young is selected for because of social benefits to the young and/or adopting parents. We propose, instead, that brood amalgamation is a function of two separate processes: brood desertion and brood adoption. To examine brood desertion, we develop a graphic model to predict when parents should abandon their young and we test this model experimentally for the Barrow's goldeneye (Bucephala islandica). As predicted, females deserted their offspring when the size of the brood was experimentally reduced. Brood adoption occurred when deserted ducklings joined other broods. However, the success of ducklings in doing so was strongly dependent on the availability of potential host broods and on the age of the recipient broods. Foreign ducklings were readily accepted into young broods (<10 d old) but invariably were rejected from old broods. We could detect no benefits or costs of brood adoption to the host females, contrary to the expectations of a social benefit hypothesis. Our experiments indicate that Crèching behavior is driven by selection on adults to abandon their brood when the benefits of continued investment are outweighed by the reduction in future reproduction and selection on deserted ducklings to join other broods to obtain parental care. Rather than a form of cooperative brood care, Crèching in goldeneyes is perhaps best considered as a form of reproductive parasitism, entailing parent-offspring conflict over brood desertion and intergenerational conflict over adoption of abandoned young.     

Effects of parental and own early developmental conditions on the phenotype in zebra finches (Taeniopygia guttata)

The performance of an individual can be critically influenced by its experience early in life as well as trans-generationally by the conditions experienced by its parents. However, it remains unclear whether or not the early experience of parents and offspring interact with each other and adapt offspring when the parental and own early environmental conditions match. Here, zebra finches (Taeniopygia guttata) that had experienced either early low or high nutritional conditions raised their offspring under either matched or mismatched nutritional conditions. Parental and offspring early conditions both separately affected the offspring’s adult phenotype, but early conditions experienced by parents and offspring did not interact as predicted. Offspring that grew up under conditions matching those their parents had experienced did not do better than those that grew up in a mismatched environment. Thus, transgenerational effects remain a lifelong burden to the offspring acting in addition to the offspring’s own early life experience. The lack of evidence for adaptive programming to matching environmental conditions may result from non-predictive environments under natural conditions in such opportunistic breeders.     

Environmental cues influence parental brood structure decisions in the burying beetle <Emphasis Type="Italic">Nicrophorus marginatus</Emphasis>

Parents evaluate multiple extrinsic and intrinsic cues when making decisions associated with reproduction. These decisions often reflect classic trade-offs between the cost of a strategy and its perceived fitness payoff. Life history theory predicts that when parents experience austere conditions, reproductive success is increased by producing fewer but larger offspring with a competitive advantage in this environment. Conversely, parents experiencing favorable conditions are expected to increase current reproductive success by favoring quantity over quality of offspring. We tested the predictions of life history theory using Nicrophorus marginatus (Coleoptera: Silphidae), a burying beetle species that exhibits infanticide during biparental care and hypervariable adult size across populations, by employing a factorial design that manipulated density and nutritional quality of food. We measured (1) the average number of offspring produced, (2) the average individual size of offspring, and (3) the sex ratio of the offspring. We found no effect of density or food quality on offspring sex ratio, but mean offspring size and number differed between low and high-density treatments. Nutritional environment interacted with density effects such that parents with access to high quality diets were able to modulate offspring size and number to match the perceived competitive environment, whereas those in poor nutritional condition appeared to exhibit physiological constraints to producing optimal brood structures.     

Sense and sensitivity: responsiveness to offspring signals varies with the parents' potential to breed again

How sensitive should parents be to the demands of their young? Offspring are under selection to seek more investment than is optimal for parents to supply, which makes parents vulnerable to losing future fitness by responding to manipulative displays. Yet, parents cannot afford to ignore begging and risk allocating resources inefficiently. Here, we show that parents may solve this problem by adjusting their sensitivity to begging behaviour in relation to their own likelihood of breeding again, a factor largely neglected in previous analyses of parent–offspring interactions. In two carotenoid-supplementation experiments on a New Zealand passerine, the hihi Notiomystis cincta, we supplemented adults to enhance their propensity to breed again, and supplemented entire broods to increase their mouth colour, thus enhancing their solicitation display. We found that adults that attempted two breeding attempts a season were largely insensitive to the experimentally carotenoid-rich gapes of their brood, whereas those that bred just once responded by increasing their rate of provisioning at the nest. Our results show that parents can strategically vary their sensitivity to begging in relation to their future reproductive potential. By restricting opportunities for offspring to influence provisioning decisions, parents greatly limit the potential for offspring to win parent–offspring conflict.     

Integration of donor DNA in bacterial conjugation

Conjugation between ¹³C¹⁵N- and ³H-labelled hybrid donors and ¹³C¹⁵N-labelled hybrid recipients of Escherichia coli gives rise to recombinant radioactive DNA of density greater than labelled hybrid. The donor radioactivity is present, in these molecules, in discrete heavy segments covalently attached to the light strand. When light radioactive Hfr cells are mated to heavy F^? cells in light medium, the donor label appears, in DNA extracted from the F^? cells, in labelled hybrid molecules. The radioactivity in these molecules is exclusively in the light strand. The insertion of donor material is thus restricted to a single newly formed strand of the recipient DNA and double-strand integrations do not occur. A temperature-sensitive recipient containing the dna B mutation ts₄₃ accumulates single-stranded Hfr DNA if mating is carried out at the nonpermissive temperature. The formation of a complementary strand in the recipient does not, therefore, appear to be necessary for continued transfer of Hfr DNA.     

Cooperation between non-relatives in a primitively eusocial paper wasp,Polistes dominula

In cooperatively breeding vertebrates, the existence of individuals that help to raise the offspring of non-relatives is well established, but unrelated helpers are less well known in the social insects. Eusocial insect groups overwhelmingly consist of close relatives, so populations where unrelated helpers are common are intriguing. Here, we focus on Polistes dominula—the best-studied primitively eusocial wasp, and a species in which nesting with non-relatives is not only present but frequent. We address two major questions: why individuals should choose to nest with non-relatives, and why such individuals participate in the costly rearing of unrelated offspring. Polistes dominula foundresses produce more offspring of their own as subordinates than when they nest independently, providing a potential explanation for co-founding by non-relatives. There is some evidence that unrelated subordinates tailor their behaviour towards direct fitness, while the role of recognition errors in generating unrelated co-foundresses is less clear. Remarkably, the remote but potentially highly rewarding chance of inheriting the dominant position appears to strongly influence behaviour, suggesting that primitively eusocial insects may have much more in common with their social vertebrate counterparts than has commonly been thought.     

Offspring recognition by mother crab spiders with extreme maternal care

Maternal care is provided by several spider species, but there are no reports of mother spiders recognizing their young, which suggests that maternal care can be exploited by unrelated individuals. Diaea ergandros, a crab spider with extreme, sacrificial maternal care, does accept unrelated spiderlings (ca. 43.9% of spiderlings) into its nest in areas of high nest density. However, a field and a laboratory experiment with mother spiders and natural and adoptive spiderlings demonstrated that mothers did recognize their own offspring. Recognition was not expressed in survival as adopted (unrelated) spiderlings had similar survival rate to that of natural offspring. Instead it was displayed in growth; mother D. ergandros caught large prey items for their own offspring, but not for adopted spiderlings, and so natural offspring grew more than adopted spiderlings. Also, mothers produced trophic oocytes, which are important for the sacrificial care that influences spiderling survival, only when they lived with their own offspring.     

Farming-out of offspring is a predominantly male tactics in a biparental mouthbrooding cichlid <Emphasis Type="BoldItalic">Perrisodus mircolepis</Emphasis>

Synopsis Intraspecific brood-mixing of a Tanganyikan biparental cichlid fish Perissodus microlepis has been attributed to farming-out, a behaviour in which a parent transport some or all of their free-swimming young in the mouth and put them under the care of other guarding parents. We conducted observations under natural conditions to understand how often farming-out occurs and which sex is the primary performer. At most brooding sites, young in a school entirely disappeared before attaining to the size of independence. At many of these sites, farming-out and its precursory behaviours by males preceded disappearance of their young. Females never performed farming-out. We proposed that farming-out by males is an alternative tactics to brood desertion to evade paternal roles for remating.     

Paternal effects in Arabidopsis indicate that offspring can influence their own size

The existence of genetic variation in offspring size in plants and animals is puzzling because offspring size is often strongly associated with fitness and expected to be under stabilizing selection. An explanation for variation in seed size is conflict between parents and between parents and offspring. However, for this hypothesis to be true, it must be shown that the offspring genotype can affect its own size. The existence of paternal effects would support this hypothesis, but these have rarely been shown. Using a diallel cross among four natural accessions of Arabidopsis thaliana we show that maternal, paternal and positional effects jointly influence seed size, number and the frequency of seed abortion. We found that seed abortion (%) depends on the combination of maternal and paternal genotypes, suggesting the existence of mate choice or epistatic incompatibility among accessions of A. thaliana. In addition, since paternal genotype explains approximately 10 per cent of the variation in seed size, we propose that A. thaliana''s offspring must influence the amount of resources allocated to themselves. Identification of paternal effects in Arabidopsis should facilitate dissection of the genetic mechanisms involved in paternal effects.     

Interspecific brood-mixing in Tanganyikan cichlids

Synopsis We collected schools of young, guarded by parents, of six common cichlid species to investigate the frequency and origin of interspecific brood-mixing. The main host species were a piscivore Lepidiolamprologus elongatus and a scale-eater Perissodus microlepis; more than half of their schools included heterospecific young, accounting for 20–40% of the total young. Most of the foreign young belonged to four biparental mouth-brooders whose parents have a habit of carrying their young in their mouths. Many of these young were smaller than the largest young brooded by their own parents. We concluded that adoption of young before independence results from farming-out, a behavior by which parents actively transfer their young to foster parents.     

On the Nature of Recombinants Formed during Transformation in Hemophilus influenzae

During the process of transformation in Hemophilus influenzae integration of donor DNA, i.e. the formation of recombinant DNA, involves the incorporation of single-stranded DNA. Evidence was obtained from cesium chloride density gradient centrifugation of DNA from donor-recipient complexes that integration was accompanied by the formation of hybrid DNA with a density intermediate with respect to heavy, ²H, ¹⁵N, donor and light, ¹H, ⁴N recipient DNA. On denaturation the position of the heavy donor DNA moved closer to, but not all the way toward, the density position of the original donor DNA. In addition to supporting the idea of single-stranded incorporation, this evidence suggested that the integrated donor DNA was covalently linked to light recipient DNA. The DNA was taken up in the double-stranded form and no detectable amounts of denatured DNA could be found during the transformation process. However, during the process of integration an amount of donor atoms, equivalent to the amount of hybrid DNA formed, appeared in recipient DNA, and indicated that while one strand of DNA was integrated the other was broken down and resynthesized. The density of the hybrid DNA, as well as rebanding of denatured hybrid, indicated that the size of the integrated piece of DNA was large, approximately 6 x 10⁶ daltons.     

Do honest signalling models of offspring solicitation apply to insects?

Honest signalling models predict that the intensity of solicitation by offspring influences the level of provisioning provided by parents and reflects offspring need. The empirical evidence supporting these predictions primarily comes from studies of birds or mammals. Thus, although parental care of altricial offspring is taxonomically widespread, the generality of these models is not well known. To investigate whether honest signalling models apply to insects, we manipulated parent and offspring behaviour in the burying beetle Nicrophorus orbicollis, a species with advanced parental care. First, within biparental care, we manipulated the brood size to alter the parents'' perception of offspring need. We measured the care giving behaviour of male and female parents to examine whether either adjusts its level of care according to offspring need. In the second experiment, because two parents together provision the brood more often than single parents, we manipulated the number of care givers (uniparental and biparental care) and measured offspring solicitation to assess whether offspring change their behaviour in response to need. Our results show that parent behaviour is broadly consistent with the first prediction of the models; both sexes provisioned larger broods more often than smaller broods. Larval solicitation was also consistent with the second prediction; larvae that were provisioned less often begged more. Our results provide evidence that honest signalling models can be applied to insects as well as vertebrates, although there are also subtle differences in care giving behaviour that may be important.     

To share or not to share: clonal integration in a submerged macrophyte in response to light stress

The ability of clonal plant species to share resources has been studied in many experiments. The submerged macrophyte Potamogeton perfoliatus produces interconnected ramets within short time intervals and hence may or may not share resources with ramets growing in less favourable microhabitats. From a genet point of view, sharing with ramets growing under less favourable conditions might not be an optimal strategy when photosynthates could be used to establish other ramets growing under more favourable conditions. To analyse the plasticity in clonal integration of P. perfoliatus, we set up a factorial aquaria experiment with unshaded or shaded recipient ramets (offspring), which were connected to or separated from donor ramets (parents). Increased biomass production of offspring in parent–offspring systems compared with severed offspring in both light and shade showed that ramets share resources through clonal integration. The relative translocation to the first- and second-offspring generation was influenced by habitat quality: If first-offspring ramets grew in a shaded microhabitat, second-offspring ramets clearly profited. This may be at least partially because of the fact that resources are shifted from first-offspring to second-offspring ramets, indicating controlled senescence of the first-offspring. This complex sharing behaviour might be relevant when plants produce ramets within a dense patch of macrophytes, where support of a shaded ramet might not pay off.     

Crowded locusts produce hatchlings vulnerable to fungal attack

Transgenerational effects of parental experience on offspring immunity are well documented in the vertebrate literature (where antibodies play an obligatory role), but have only recently been described in invertebrates. We have assessed the impact of parental rearing density upon offspring disease resistance by challenging day-old locust hatchlings (Schistocerca gregaria) from either crowd- or solitary-reared parents with the fungal pathogen Metarhizium anisopliae var. acridum. When immersed in standardized conidia suspensions, hatchlings from gregarious parents suffered greater pathogen-induced mortality than hatchlings from solitary-reared parents. This observation contradicts the basic theory of positive density-dependent prophylaxis and demonstrates that crowding has a transgenerational influence upon locust disease resistance.     

Competence Mutant of Haemophilus influenzae with Abnormal Ratios of Marker Efficiencies in Transformation

In studies of competence-deficient mutants of Haemophilus influenzae which absorb deoxyribonucleic acid (DNA) but fail to produce transformants, it was observed that in some mutants the residual transforming activity for different markers varied widely, i.e., produced a ratio effect. One of these mutants, com⁻⁵⁶, was studied intensively to determine the cause of the residual efficiency of transformation and the reason for the ratio effect. The residual frequency of transformation was higher for markers considered single-site mutations (like naladixic acid resistance), whereas the least efficient markers tested were those conferring resistance to high levels of streptomycin or novobiocin which are more complex than single-site mutations. Measurement of frequencies of cotransformation indicated that overall genetic linkage was reduced. Transfection was fairly efficient with phage S2 DNA, but not prophage DNA. Donor marker activity could be detected in transformed cell lysates, but not linked to recipient markers in recombinant molecules. Sucrose gradient analysis of such lysates revealed that donor material was associated with recipient DNA in at least normal quantities, but lacked detectable genetic activity. Material from donor DNA labeled with heavy isotopes was incorporated into recipient chromosomal fragments having a density indistinguishable from normal density, unlike the hybrid density recombinant material found in normal cells. No excessive solubilization or nicking of unincorporated donor was detected. It is postulated that this strain contains a hyperactive nuclease, which reduces the effective size of the input DNA during the integration process.     

The power of the seasons: rainfall triggers parental care in poison frogs

The quality of breeding sites is of great importance for the reproductive success and accordingly the fitness of many animal species. Hence, individuals should decide carefully where to rear their offspring. Often parents have to account for multiple characteristics of habitat quality at once, which in turn might change over time. Specimens confronted with such variability may evolve the ability to display context-dependant decision plasticity. Anuran amphibians breeding in ephemeral pools largely face two risks for their offspring: desiccation and predation. The Neotropical poison frog Ranitomeya variabilis deposits both eggs and tadpoles in phytotelmata. These small tadpole nurseries lower the risk of offspring predation. However, because most poison frog tadpoles are cannibalistic, even these pools need to be surveyed for predators, and parents tend to avoid deposition with conspecifics. We tested if this avoidance behaviour does change in parental R. variabilis depending on seasonal circumstances. Over several months we provided the frogs the option to deposit their eggs or tadpoles in pools that did and did not contain chemical cues of cannibalistic conspecifics, respectively. During the rainy season, frogs strongly avoided conspecific cues for both eggs and tadpoles. Anyway, with the change to the dry season, parental preferences changed such that parent frogs were more likely to deposit tadpoles (but not eggs) in pools containing cues of conspecific tadpoles. We suggest that R. variabilis, a species that typically isolates its cannibalistic offspring, has evolved a plastic feeding behaviour with regard to the risk of phytotelmata desiccation. We interpret that parents provide older tadpoles with younger ‘trophic’ tadpoles in order to accelerate their development and save them from impending desiccation.