Mode Of Parental Care Research Articles

Comparative studies need to rely both on sound natural history data and on excellent statistical analysis.

We certainly agree with Schradin [1] that comparative studies need to use the best information available—as well as clear definitions, up-to-date statistical techniques and common sense. We have divided our response into two sections: the first dealing with Schradin's critique of our 2017 paper and the classification of the social organization of shrews; the second dealing with three general issues that his commentary raises. The paper that Schradin is commenting on [2] asks whether cooperative breeders (which we define as species where non-breeding helpers assist breeders to raise their young) in mammals are more commonly found in arid environments than monogamous species (defined as species where breeding pairs of males and females remain together for more than one season) from which cooperative breeders appear to be derived [3]. It shows that, as in birds, cooperative breeders tend to live in relatively arid habitats compared to monogamous species. As we describe below, these conclusions are unaffected by differences between our classification of the social organization of shrews and the classification suggested by Schradin. Schradin's first criticism is that the categorizations of shrews that we have used in this analysis were based on one paper on a single species. This is incorrect, for our categorization of shrews was based on more than 70 separate sources (see electronic supplementary material, appendix S1). When we published our dataset [4], we were required to reduce the associated reference list by the editors of the journal and, to comply, we removed around 75% of our 2000+ sources, often listing a single reference per species or group of species, and frequently using generic reviews for particular groups where these were available: for example, for many rodent species, we simply listed Wolff and Sherman's Rodent Societies [5], and …

Reproductive behaviour of two tilapia species (Oreochromis niloticus, Linné, 1758; Sarotherodon melanotheron, Rüppel, 1852) in freshwater intra and interspecific pairing context

Nile tilapia Oreochromis niloticus (NT) and Black-chinned tilapia Sarotherodon melanotheron (BCT) are respectively characterized by fast growth and water salinity tolerance which attract the farmers who could take advantage of both species characteristics by producing hybrids reared in brackish or marine waters. Little information is however available about social interactions between the two species which are distinct by their mode of parental care (oral incubation). The objective of this study was to determine the behaviour of the two species, NT and BCT placed in freshwater intraspecific and interspecific pairing contexts. Females of both species (n=20 per species) were first isolated for 90days in a 60L aquarium to determine the average duration between spawning in the absence of males. With the approach of 4th spawning or after 90days of isolation, intra and interspecific pairing (fish average weight 200.4±5.1g) were made 10 times by pairing mode in a 350L aquarium. The day after fish pairing, 15min videos were recorded at one hour intervals from 8:00h to 17:00h, and courtship and aggressiveness behaviour were quantified. The results showed that isolated NT females had an average duration between two spawning of 15.9days. No spawning was observed in BCT females. Spawning events were observed in the NT intraspecific pairs, with strictly maternal oral egg incubations. Behavioural differences and some similarities were noted between the two species. NT male was the most dominant in front of females of both species and NT females showed dominance on BCT males. No clear hierarchy was observed in BCT pairs. Courtship behaviours were observed in all pairings with longer durations in NT pairs. Nest building was observed from 8:00h to 17:00h in both sexes of BCT and male NT. NT females built nests from 11:00h with longer durations when paired with males BCT than when paired with their conspecific males. These first results, reflecting behavioural plasticity in both species suggested that other breeding conditions favouring less aggressive behaviour could lead to a natural interspecific hybridization between NT and BCT.

Multi-Generational Kinship, Multiple Mating, and Flexible Modes of Parental Care in a Breeding Population of the Veery (Catharus fuscescens), a Trans-Hemispheric Migratory Songbird.

We discovered variable modes of parental care in a breeding population of color-banded Veeries (Catharus fuscescens), a Nearctic-Neotropical migratory songbird, long thought to be socially monogamous, and performed a multi-locus DNA microsatellite analysis to estimate parentage and kinship in a sample of 37 adults and 21 offspring. We detected multiple mating in both sexes, and four modes of parental care that varied in frequency within and between years including multiple male feeders at some nests, and males attending multiple nests in the same season, each with a different female. Unlike other polygynandrous systems, genetic evidence indicates that multi-generational patterns of kinship occur among adult Veeries at our study site, and this was corroborated by the capture of an adult male in 2013 that had been banded as a nestling in 2011 at a nest attended by multiple male feeders. All genotyped adults (n = 37) were related to at least one other bird in the sample at the cousin level or greater (r ≥ 0.125), and 81% were related to at least one other bird at the half-sibling level or greater (r ≥ 0.25, range 0.25–0.60). Although our sample size is small, it appears that the kin structure is maintained by natal philopatry in both sexes, and that Veeries avoid mating with close genetic kin. At nests where all adult feeders were genotyped (n = 9), the male(s) were unrelated to the female (mean r = -0.11 ± 0.15), whereas genetic data suggest close kinship (r = 0.254) between two male co-feeders at the nests of two females in 2011, and among three of four females that were mated to the same polygynous male in 2012. To our knowledge, this is the first evidence of polygynandry occurring among multiple generations of close genetic kin on the breeding ground of a Nearctic-Neotropical migratory songbird.

Embryo oxygenation in pipefish brood pouches: novel insights

The pipefish brood pouch presents a unique mode of parental care that enables males to protect, osmoregulate, nourish and oxygenate the developing young. Using a very fine O2 probe, we assessed the extent to which males of the broad-nosed pipefish (Syngnathus typhle) oxygenate the developing embryos and are able to maintain pouch fluid O2 levels when brooding in normoxia (100% O2 saturation) and hypoxia (40% O2 saturation) for 24 days. In both treatments, pouch fluid O2 saturation levels were lower compared with the surrounding water and decreased throughout the brooding period, reflecting greater offspring demand for O2 during development and/or decreasing paternal ability to provide O2 to the embryos. Male condition (hepatosomatic index) was negatively affected by hypoxia. Larger males had higher pouch fluid O2 saturation levels compared with smaller males, and levels were higher in the bottom section of the pouch compared with other sections. Embryo size was positively correlated with O2 availability, irrespective of their position in the pouch. Two important conclusions can be drawn from our findings. First, our results highlight a potential limitation to brooding within the pouch and dismiss the notion of closed brood pouches as well-oxygenated structures promoting the evolution of larger eggs in syngnathids. Second, we provide direct evidence that paternal care improves with male size in this species. This finding offers an explanation for the documented strong female preference for larger partners because, in terms of oxygenation, the brood pouch can restrict embryo growth.

Temporal and Spatial Complexity of Maternal Thermoregulation in Tropical Pythons

Parental care is a widespread adaptation that evolved independently in a broad range of taxa. Although the dynamics by which two parents meet the developmental needs of offspring are well studied in birds, we lack understanding about the temporal and spatial complexity of parental care in taxa exhibiting female-only care, the predominant mode of parental care. Thus, we examined the behavioral and physiological mechanisms by which female water pythons Liasis fuscus meet a widespread developmental need (thermoregulation) in a natural setting. Although female L. fuscus were not facultatively thermogenic, they did use behaviors on multiple spatial scales (e.g., shifts in egg-brooding postures and surface activity patterns) to balance the thermal needs of their offspring throughout reproduction (gravidity and egg brooding). Maternal behaviors in L. fuscus varied by stage within reproduction and were mediated by interindividual variation in body size and fecundity. Female pythons with relatively larger clutch sizes were cooler during egg brooding, suggesting a trade-off between reproductive quantity (size of clutch) and quality (developmental temperature). In nature, caregiving parents of all taxa must navigate both extrinsic factors (temporal and spatial complexity) and intrinsic factors (body size and fecundity) to meet the needs of their offspring. Our study used a comprehensive approach that can be used as a general template for future research examining the dynamics by which parents meet other developmental needs (e.g., predation risk or energy balance).

Characterisation of nine microsatellite loci in the caecilian amphibian Boulengerula uluguruensis (Gymnophiona), and their cross-species utility in three congeneric species

We characterise nine polymorphic microsatellites for the caecilian amphibian Boulengerula (cf.) uluguruensis. We found between five and 13 alleles per locus in 17 individuals from six sites across four Eastern Arc Mountain blocks and coastal forest in Tanzania. In the population with the largest sample size (Uluguru North, n = 8), two loci deviated from Hardy–Weinberg equilibrium. We also report cross-species utility of these markers in three other Boulengerula species (B. taitanus, B. niedeni, and B. boulengeri), and populations representing potentially undescribed species, approximately proportionate to their phylogenetic divergence from B. uluguruensis. The loci have the potential to quantify reproductive success (in view of skin feeding, a unique mode of parental care) and to determine the genetic structure of local populations, providing vital information for conservation studies of this endangered and little studied genus.

Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae)

Dendrobatid frogs perform a unique mode of parental care, ranging from egg attendance and tadpole transport to tadpole feeding. It is hypothesized that a behaviour in which the egg attending parent remains with the cluch is the most primitive condition. In more advanced forms or parental care, the male is able to attend several clutches of eggs. Tadpole attendance and feeding, finally, started as deceit; the male induced the female to lay eggs into a bromeliad leaf axil already occupied by a larva. Costs and benefits of the different modes of parental care and possible alternative reproductive tactics are discussed.

The evolution of reproductive and genomic diversity in ray‐finned fishes: insights from phylogeny and comparative analysis

Collectively, ray‐finned fishes (Actinopterygii) display far more diversity in many reproductive and genomic features than any other major vertebrate group. Recent large‐scale comparative phylogenetic analyses have begun to reveal the evolutionary patterns and putative causes for much of this diversity. Several such recent studies have offered clues to how different reproductive syndromes evolved in these fishes, as well as possible physiological and genomic triggers. In many cases, repeated independent origins of complex reproductive strategies have been uncovered, probably reflecting convergent selection operating on common suites of underlying genes and hormonal controls. For example, phylogenetic analyses have uncovered multiple origins and predominant transitional pathways in the evolution of alternative male reproductive tactics, modes of parental care and mechanisms of sex determination. They have also shown that sexual selection in these fishes is repeatedly associated with particular reproductive strategies. Collectively, studies on reproductive and genomic diversity across the Actinopterygii illustrate both the strengths and the limitations of comparative phylogenetic approaches on large taxonomic scales.

Proteomics profiling of epidermal mucus secretion of a cichlid (Symphysodon aequifasciata) demonstrating parental care behavior

The discus fish (Symphysodon aequifasciata) is a cichlid demonstrating advanced mode of parental care towards fry. Both male and female fish utilized epidermal mucus secreted from specialized epidermal cells to feed developing fry. We utilized proteomics to compare protein profile from parental and nonparental fish. Gel analysis revealed a total of 35 spots that were up-regulated in parental mucus. In tandem, another 18 spots were uniquely expressed in parental mucus. MS analysis of these spots identified proteins such as fructose biphosphate aldolase, nucleoside diphosphate kinase, and heat shock proteins, which are essential to support energy provision, cell repair and proliferation, stress mediation, and defense mechanism in parental fish during parental-care period. Concurrently, the detection of several antioxidant-related proteins such as thioredoxin peroxidase and hemopexin suggests a need to overcome oxidative stress during hypermucosal production in parental-care behavior. A C-type lectin was also found to be uniquely expressed in parental mucus and could have important role in providing antimicrobial defense to both parental fish and fry. In summary, our study shows that discus mucus proteome undergoes changes in protein expression during parental-care period.

Prevalence of different modes of parental care in birds

Estimates of the incidence of major classes of parental care by birds are drawn from classical studies that preceded both the publication of a massive secondary literature and the revolution driven by molecular approaches to avian phylogeny. Here, I review this literature in the light of new phylogenetic hypotheses and estimate the prevalence of six distinct modes of care: use of geothermal heat to incubate eggs, brood parasitism, male only care, female only care, biparental care and cooperative breeding. Female only care and cooperative breeding are more common than has previously been recognized, occurring in 8 and 9% of species, respectively. Biparental care by a pair-bonded male and female is the most common pattern of care but at 81% of species, the pattern is less common than once believed. I identify several problems with existing hypotheses for the evolution of parental care and highlight a number of poorly understood contrasts which, once resolved, should help elucidate avian social evolution.

The origin of parental care in birds: a reassessment

The origin of parental care in birds: a reassessment

A new mode of parental care in cockroaches

A new form of maternal provisioning of newly hatched nymphs is described in the ovoviviparous cockroach Gromphadorhina portentosa. Shortly after expelling the hatching egg case, the female exudes from her abdominal tip a whitish, translucent material on which neonates actively feed. Integumentary gland cells lining the brood sac are the most likely source of the secretion. This form of maternal provisioning may not be restricted to the Madagascar hissing cockroach; a glandular brood sac similar to that of G. portentosa is found in at least three additional ovoviviparous cockroaches.

Animal behavior: male parenting of New Guinea froglets.

Male parental care is exceptionally rare in nature, although one of the most fascinating aspects of New Guinea's biodiversity is the evolution of male care in the frog family Microhylidae. Here I report a new mode of parental care: transport of froglets by the male parent, which was recently discovered in two species of microhylid frogs from the mountains of Papua New Guinea. As the offspring jump off at different points, they may benefit from reduced competition for food, lower predation pressure and fewer opportunities for inbreeding between froglets, which may explain why this unusual form of parental care evolved.

Biparental care in the tadpole-feeding Amazonian treefrog Osteocephalus oophagus

AbstractThe Central Amazonian treefrog Osteocephalus oophagus breeds in water-filled bromeliad or palm tree leaf axils or in treeholes. The larvae feed on eggs provided by their parents; larvae not provided with eggs die. Survival of the larvae is ensured by the fact that the pair always spawns at the same site. They return at intervals of 5 to 7 days. Pair bonding is the rule in areas with low frog densities. The first eggs develop into tadpoles and later clutches of fertilized eggs serve as food. There is no apparent communication system between larvae and mother. After metamorphosis of the larvae the pair continues to lay eggs into the same leaf axils and these eggs also develop into tadpoles. This behavior is compared to that of other frogs that feed their tadpoles on eggs. It seems to be the least advanced mode of parental care involving tadpole feeding and demonstrates one of the initial steps that has led to more complex parental care behaviors in frogs.

Parental care as a game

AbstractA new game model of parental care is presented where fitnesses of males and females depend on frequencies of care and no‐care strategies in the population, as well as strategies of individuals and those of their mates. Evolutionarily stable states (ESS) of biparental‐care (BC), female‐care (FC), male‐care (MC), and no‐care (NC) are represented as regions in a 3‐dimensional parameter space, comprising the ratio of the number of offspring raised by FC or MC to that by BC, the ratio of that by NC to that by FC or MC, and the sex ratio. ESSs are not necessarily uniquely determined: ESS regions of FC and MC overlap in parts, as well as those of BC and NC. In a region where none of the four states is ever an ESS, a polymorphism (a mixed state of care and no‐care strategies in one or both sexes) is stable. Although an asymmetry between prezygotic investment times of males and females results in the difference in sizes of the ESS regions of FC and MC, it is not responsible for determining whether FC or MC evolves from other modes of parental care as a result of slowly changing parameters. The key factor is the sex ratio of adults in the population. By a slightly modified model, it is also shown that paternity uncertainty at fertilization of eggs is highly important for evolution of FC.

PLASTICITY OF JAW AND SKULL MORPHOLOGY IN THE NEOTROPICAL CICHLIDS GEOPHAGUS BRASILIENSIS AND G. STEINDACHNERI.

I examined plasticity of jaw and skull morphology induced by feeding different diets in two species of the neotropical cichlid genus Geophagus. The two species possess different modes of development, which affect the size at which young begin feeding. I hypothesized that the difference in size at first feeding could lead to a difference in the amount of change inducible in the two species. The young of the substrate-spawning species, G. brasiliensis, which begin feeding at a smaller size, were predicted to be more plastic than those of the mouthbrooding species, G. steindachneri. The two diets used to induce differences were brine shrimp nauplii and chironomid larvae. Numerous measures of the jaw and skull differed significantly between groups fed the two diets but the amount of plasticity induced was small and would not present a problem for taxonomists. Contrary to my prediction, both the magnitude and pattern of plasticity induced in the two species was similar. Thus, mode of parental care and the size at which young begin feeding do not affect the degree of plasticity. Fish fed brine shrimp nauplii were longer in oral jaw region, but were shorter and shallower in the area behind the oral jaws. An additional group of G. brasiliensis was fed flake food to compare the results of this study to other studies. The differences in measures between fish fed brine shrimp diets and flake food diets were greater than those between fish fed brine shrimp and chironomid larvae. A possible role of plasticity for enhancing rather than retarding morphological evolution is discussed.