Evolutionary transitions in parental care and live bearing in vertebrates

We provide the first review of phylogenetic transitions in parental care and live bearing for a wide variety of vertebrates. This includes new analyses of both numbers of transitions and transition probabilities. These reveal numerous transitions by shorebirds and anurans toward uniparental care by either sex. Whereas most or all of the shorebird transitions were from biparental care, nearly all of the anuran transitions have been from no care, reflecting the prevalence of each form of care in basal lineages in each group. Teleost (bony) fishes are similar to anurans in displaying numerous transitions toward uniparental contributions by each sex. Whereas cichlid fishes have often evolved from biparental care to female care, other teleosts have usually switched from no care to male care. Taxa that have evolved exclusive male care without courtship-role reversal are characterized by male territoriality and low costs of care per brood. Males may therefore benefit from care through female preference of parental ability in these species. Primates show a high frequency of transitions from female care to biparental care, reflecting the prevalence of female care in basal lineages. In the numerous taxa that display live bearing by females, including teleosts, elasmobranchs, squamate reptiles and invertebrates, we find that live bearing has always evolved from a lack of care. Although the transition counts and probabilities will undoubtedly be refined as phylogenetic information and methodologies improve, the overall biases in these taxa should help to place adaptive hypotheses for the evolution of care into a stronger setting for understanding directions of change.     

Survival of broods under parental care and parental roles of the cichlid fish,Lamprologus toae,in Lake Tanganyika

The survival of offspring guarded by both parents and by only the female parent who remained after experimental removal of the male parent was observed in the cichlid fishLamprologus toae in its natural habitat. The number of offspring guarded by both parents abruptly decreased during the period from eggs through postlarvae. It became stable for low rate of mortality when the offspring were between 0.5 and 1.8 cm in body length. The number again decreased this time gradually after attaining 1.8 cm in body length. Mortality seemed to be caused by predation. Experimental removal of the male parent at any larval stage caused the decrease of offspring by predatory fishes. It seems that both parents are indispensable to protect the offspring against predators under natural conditions.     

Isotocin regulates paternal care in a monogamous cichlid fish

While the survival value of paternal care is well understood, little is known about its physiological basis. Here we investigate the neuroendocrine contributions to paternal care in the monogamous cichlid, Amatitlania nigrofasciata. We first explored the dynamic range of paternal care in three experimental groups: biparental males (control fathers housed with their mate), single fathers (mate removed), or lone males (mate and offspring removed). We found that control males gradually increase paternal care over time, whereas single fathers increased care immediately after mate removal. Males with offspring present had lower levels of circulating 11-ketotestosterone (11-KT) yet still maintained aggressive displays toward brood predators. To determine what brain regions may contribute to paternal care, we quantified induction of the immediate early gene c-Fos, and found that single fathers have more c-Fos induction in the forebrain area Vv (putative lateral septum homologue), but not in the central pallium (area Dc). While overall preoptic area c-Fos induction was similar between groups, we found that parvocellular preoptic isotocin (IST) neurons in single fathers showed increased c-Fos induction, suggesting IST may facilitate the increase of paternal care after mate removal. To functionally test the role of IST in regulating paternal care, we treated biparental males with an IST receptor antagonist, which blocked paternal care. Our results indicate that isotocin plays a significant role in promoting paternal care, and more broadly suggest that the convergent evolution of paternal care across vertebrates may have recruited similar neuroendocrine mechanisms.     

Tidal cycling and parental behavior of the cichlid fish,Biotodoma cupido

Synopsis Parental behavior of the substrate-brooding cichlid, Biotodoma cupido, was studied in a small creek entering the lower Essequibo River, Guyana, where the freshwaters are affected by semi-diurnal tides. Physico-chemical variables of the tidal cycle were associated with the parental behavior of B. cupido. During late ebb and early flood tides, while off-spring were nest dependent, parents displayed intense aggression toward brood predators, mainly characins. At low tide, when the concentration of dissolved oxygen decreased to about 4 mg 1^–1 and that of free carbon dioxide increased to 28 mg 1^–1, parents entered a state of somnolence and brood predators vanished. Early flood tide brought an immediate and dramatic reversal of hypoxic and hypercarbic conditions and an associated renewal of aggressive and predatory activity. At very low tide, parents orally transferred the brood to a secondary nest depression in deeper water. The significance of water-level fluctuation to the evolution of this behavior, as well as that of parent-brood itineracy and the related phenomena of oral incubation and movable nests, is discussed.     

Influence of brood size and offspring size on parental investment in a biparental cichlid fish,Neolamprologus moorii

Both males and females ofNeolamprologus moorii, a substrate-spawning cichlid fish in Lake Tanganyika, tend their eggs and fry. In this study, the influence of brood size and fry size on parental investment of this species was examined under natural conditions. Breeding parents intensively attacked fry-eating fishes that approached their broods. The attack rate by the parents against the approaching fry-eaters was positively correlated with brood size and negatively with fry size, but was much more strongly related to brood size. This suggests that the parental decision for brood defense appeared to be primarily determined by brood size. The reason for fry size being less important in the parental decision may be that even large fry have a low survival ability on their own under the high predation pressure in the study sites.     

Probing aggressive motivation in a cichlid fish

The duration of startles provides an inverse measure of motivation to resume the previous activity. Here, we use a novel method in which one convict cichlid fish (Amatitlania nigrofasciata) of a competing pair was startled independently of the opponent. Fish were given various opponents and the mean startle duration determined. This mean was negatively correlated with the mean use of highly escalated ‘frontal activities’ such as biting and frontal display, but not the less escalated lateral displays or tail beating. Thus the startle duration was a reliable surrogate measure of the most escalated components of aggressive interactions. That is, it provided a motivational probe for aggressiveness of individual fish. Fight motivation is often determined in terms of fight duration or physiological costs for losers, who reveal the costs they are prepared to pay. We discuss various potential advantages of the motivational probe over previous measures, particularly with respect to winners and losers and different times during the interactions.     

Pedigree reconstruction in wild cichlid fish populations

It is common practice to use microsatellites to detect parents and their offspring in wild and captive populations, in order to reconstruct a pedigree. However, correct inference is often constrained by a number of factors, including the absence of demographic data and ignorance regarding the completeness of parental sampling. Here we present a new Bayesian estimator that simultaneously estimates the pedigree and the size of the unsampled population. The method is robust to genotyping error, and can estimate pedigrees in the absence of demographic data. Using a large-scale microsatellite assay in four wild cichlid fish populations of Lake Tanganyika (1000 individuals in total), we assess the performance of the Bayesian estimator against the most popular assignment program, Cervus. We found small but significant pedigrees in each of the tested populations using the Bayesian procedure, but Cervus had very high type I error rates when the size of the unsampled population was assumed to be lower than what it was. The need of pedigree relationships to infer adaptive processes in natural populations places strong constraints on sampling design and identification of multigenerational pedigrees in natural populations.     

Dynamics of female choice for parental care in a fish species where care is facultative

In the peacock wrasse (Symphodus tinca), females either placetheir eggs in a nest under the care of a male or disperse theireggs widely so that they receive no protection. The same femalecan spawn in both modes. Females appear to prefer males withnests early in the nesting cycle, and they spawn less oftenthan expected in late-cycle nests and with non-nesting males.Survival and hatching success are consistently higher for eggsplaced in early nests, particularly in mid-season when egg predationis intense and hatching times are relatively long. Nevertheless,30%-80% of females place their eggs outside nests, even whenhatching success is more than four times greater with care.A model incorporating search time for nests correctly predictedthe qualitative changes in the tendency of females to choosecare or no care over the course of the mating season. Extensionsof the model suggest that in the early part of the season, whennests are rare and the relative survival advantage of parentalcare is small, females should sample no more than one nest beforeopting for no care. In mid-season, when the advantages of careare highest and between-nest travel times are low, females areestimated to visit at least 8 nests before abandoning the effort,corresponding to a giving-up time of about 43 min of search.Later in the season, when short hatching times reduce the relativebenefit of care, females are estimated to visit between 4 and5 nests before giving up, corresponding to about 31 min of search.We suggest that the variability in parental care in this speciesarises from seasonal changes in relative costs and benefitsof care for the two sexes.     

GnRH-systems in the forebrain of cichlid fish.

The neuronal systems that contain gonadotropin-releasing hormone (GnRH) were quantitatively examined in the forebrain of two cichlid species (Oreochromis niloticus Lin. and Tilapia maria Boulenger) using tracing methods and immunostaining. In both species the nucleus olfacto-retinalis and a population of neurons in the basal preoptic region contained GnRH. The nucleus olfacto-retinalis was divided into several neuronal subpopulations which differed with respect to cytology, projection pattern, and peptide content. GnRH cell number increased with body size, the rates being different for the different subpopulations. A sexual dimorphism was found in the basal preoptic region of Tilapia; males had significantly fewer GnRH-containing cells than females. Selective staining of the basal preoptic region demonstrated that this cell group is the main source of GnRH-innervation of the pituitary gland and indicate that the molecular forms of GnRH expressed in the two cell populations studied may be different.     

Evolutionary history of Lake Tanganyika's scale-eating cichlid fishes

Although Lake Tanganyika is not the most species-rich of the Great East African Lakes it comprises by far the greatest diversity of cichlid fishes in terms of morphology, ecology, and breeding styles. Our study focuses on the Tanganyikan cichlid tribe Perissodini, which exhibits one of the most peculiar feeding strategies found in cichlids-scale-eating. Their evolutionary history was reconstructed from 1416 bp DNA sequence of two mitochondrial genes (ND2 and partial control region) and from 612 AFLP markers. We confirm the inclusion of the zooplanktivorous genus Haplotaxodon in the tribe Perissodini, and species status of Haplotaxodon trifasciatus. Within the Perissodini, the major lineages emerged within a short period roughly 1.5-2 MYA, which makes their radiation slightly younger than that of other Tanganyikan cichlid tribes. Most scale-eaters evolved in deep-water habitat, perhaps associated with the previously documented radiations of other deep-water dwelling cichlid lineages, and colonized the shallow habitat only recently.     

Climate and body size influence nest survival in a fish with parental care

1. The current study examined the effect of broad-scale climate and individual-specific covariates on nest survival in smallmouth bass over a 20-year period. 2. Large-scale climate indices [winter North Atlantic Oscillation (NAO) and winter El Ni?o/Southern Oscillation (ENSO)] and body size of parental males were important covariates in nest survival along with nest age and a quadratic trend in survival. 3. We did not find an effect due to a habitat covariate (total effective fetch) or a phenology covariate (degree-days at start of nesting) on nest survival. 4. Male size in the second half of the nesting season was a more influential covariate on nest success than male size in the first half or throughout the nesting period. 5. We present evidence showing that winter NAO/ENSO indices establish limnological conditions the following spring that influence thermal stability of the lake during the nesting period. 6. The combined climate and body size covariates point to nest survival as a function of lagged climate-scale influences on limnology and the individual-scale influence of bioenergetics on the duration of parental care and nest success.     

Evolutionary transitions in protein fold space

With the number of known protein folds potentially approaching completion, the problems associated with their systematic classification are evaluated. It is argued that it will be difficult, if not impossible, to find a general metric based on pairwise comparison that will provide a satisfactory classification. It is suggested that some progress may be made through comparison against a library of idealised 'template' folds, but a proper solution can only be attained if this includes a model of the underlying evolutionary processes. These processes are considered with examples of some unexpected relationships among folds, including circular permutations. The problem is finally set in the wider context of the genetic environment, introducing complications relating to introns, gene fixation and population size.     

Maternal care and altered social phenotype in a recently collected stock of Astatotilapia burtoni cichlid fish

For over 30 years, the African cichlid fish, Astatotilapia burtoni, has been an important model system for studying the mechanisms underlying socially mediated behavioral change, with the focus being the dominance behavior of males. A recently collected wild-stock (WS) of this species invigorates interest in parallel studies of females' behavior. Here, we describe a robust 'good-mother' phenotype, increased maternal affiliation in fry, and subtle differences in males' behavior that are exhibited by this new stock. While the females of both the laboratory-stock (LS) and the WS brood the developing fry in their buccal cavity, only the WS continues to provide maternal care after initial release of the fry while the LS engage in filial cannibalism. We show that weight loss during starvation, either during brooding or with restriction of food, is greater in the LS than in the WS; thus, the observed behavioral differences may be tied to metabolic differences. The WS also exhibits a robust androgen response to challenge during the maternal care phase. Given the increasing power of genomic tools available for this species, the comparison of these two stocks will offer the opportunity to investigate the genetic and genomic basis of behavioral differences.     

Depth equilibration of a shallow-water cichlid fish

The cichlid Melanochromis exasperatus has a natural distribution which is restricted to a single island in Lake Malawi, Africa. Diving observations indicated that it does not occur below 4.5 m depth. Measurements of depth equilibration in a pressure tank showed that males can equilibrate to a depth of 25 m and females to 18 m. Mean maximum sustained rate of depth equilibration was 2 m day⁻¹. M. exasperatus survived a pressure decrease of 40% every 12 h from the maximum equilibration depth to the surface. The fish swim actively during the day but rest on the bottom at night when they are equilibrated to a depth 1 m deeper than ambient. Reduced activity at night is reflected in a drop in oxygen consumption to nearly half of the daytime active value.     

A test of time-place learning in a cichlid fish

This paper presents a test of time-place learning in fish. Convict cichlids, Cichlasoma nigrofasciatum, were offered food several times a day for 10–30 consecutive days. A signal was given 1 min before each food presentation. If the food was always delivered in the same corner of the aquarium, the fish spent 66% of their time in that corner after the signal was given. But if the food was given in different corners throughout the day, each corner being associated with a specific daily time, the fish failed to show preference for the target corner, even after 30 days. Instead they learned which corners yielded food at any time of the day and visited these corners successively after the feeding signal was given. Failure to associate time and place may have been caused by a low cost of travel between corners, a limited number of rewards each day, and / or interference from learning the signal-food association.     

Social familiarity modulates personality trait in a cichlid fish

Personality traits, such as exploration–avoidance, are expected to be adaptive in a given context (e.g. low-risk environment) but to be maladaptive in others (e.g. high-risk environment). Therefore, it is expected that personality traits are flexible and respond to environmental fluctuations, given that consistency across different contexts is maintained, so that the relative individual responses in relation to others remains the same (i.e. although the magnitude of the response varies the differences between high and low responders are kept). Here, we tested the response of male cichlid fish (Oreochromis mossambicus) to a novel object (NO) in three different social contexts: (i) social isolation, (ii) in the presence of an unfamiliar conspecific, and (iii) in the presence of a familiar conspecific. Males in the familiar treatment exhibited more exploratory behaviour and less neophobia than males in either the unfamiliar or the social isolation treatments. However, there were no overall correlations in individual behaviour across the three treatments, suggesting a lack of consistency in exploration–avoidance as measured by the NO test in this species. Moreover, there were no differences in cortisol responsiveness to an acute stressor between the three treatments. Together, these results illustrate how behavioural traits usually taken as measures of personality may exhibit significant flexibility and lack the expected consistency across different social contexts.