Territorial behaviour of the male johnny darter,Etheostoma nigrum

Synopsis A field study was undertaken to describe the territorial behaviour of male johnny darters (Etheostoma nigrum) over the reproductive cycle. While defending eggs, males performed fewer Lateral Displays and lost fewer encounters with conspecific males than in the pre-egg phase. As the reproductive cycle progressed males were less responsive to females and performed relatively fewer courtship and more aggressive displays. Nesting males apparently shifted from a sexual to a parental phase shortly after acquiring eggs.Frequency of response, responsiveness (number of responses/number of intrusions x 100) and maximum distance of response (MDR) of male johnny darters were highest early in the reproductive cycle and decreased over the egg-guarding phase. The patterns of territorial defence exhibited by male johnny darters over the reproductive cycle were similar to those of other species of fish with paternal care.     

Phylogenetic perspectives in the evolution of parental care in ray-finned fishes

Among major vertebrate groups, ray-finned fishes (Actinopterygii) collectively display a nearly unrivaled diversity of parental care activities. This fact, coupled with a growing body of phylogenetic data for Actinopterygii, makes these fishes a logical model system for analyzing the evolutionary histories of alternative parental care modes and associated reproductive behaviors. From an extensive literature review, we constructed a supertree for ray-finned fishes and used its phylogenetic topology to investigate the evolution of several key reproductive states including type of parental care (maternal, paternal, or biparental), internal versus external fertilization, internal versus external gestation, nest construction behavior, and presence versus absence of sexual dichromatism (as an indicator of sexual selection). Using a comparative phylogenetic approach, we critically evaluate several hypotheses regarding evolutionary pathways toward parental care. Results from maximum parsimony reconstructions indicate that all forms of parental care, including paternal, biparental, and maternal (both external and internal to the female reproductive tract) have arisen repeatedly and independently during ray-finned fish evolution. The most common evolutionary transitions were from external fertilization directly to paternal care and from external fertilization to maternal care via the intermediate step of internal fertilization. We also used maximum likelihood phylogenetic methods to test for statistical correlations and contingencies in the evolution of pairs of reproductive traits. Sexual dichromatism and nest construction proved to be positively correlated with the evolution of male parental care in species with external fertilization. Sexual dichromatism was also positively correlated with female-internal fertilization and gestation. No clear indication emerged that female-only care or biparental care were evolutionary outgrowths of male-only care, or that biparental care has been a common evolutionary stepping stone between paternal and maternal care. Results are discussed in the context of prior thought about the evolution of alternative parental care modes in vertebrates.     

The reproductive behaviour of Pogonophryne scotti confirms widespread egg-guarding parental care among Antarctic notothenioids

In this paper, the first documentation of egg-guarding behaviour in an artedidraconid species, Pogonophryne scotti, through in situ photographic imagery obtained during video transects is provided. The male specimen was observed closely guarding a well-defined multi-layered egg mass deposited on the sea floor at 240 m on the southern South Orkney Islands shelf in the northern Weddell Sea. Egg-guarding parental care is present in species that are distributed among all of the major lineages of Antarctic notothenioids; however, lack of information on egg-deposition behaviours in Bovichtidae and Pseudaphritis prevents assessment of whether parental care originated prior to the origin of the Antarctic notothenioid radiation.     

Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny

In contrast to the majority of vertebrate species, primary male parental care is common in fishes and encompasses a remarkable diversity of adaptations. Seahorses and pipefishes (Family Syngnathidae) exhibit some of the most specialized forms of paternal care in animals and so are ideally suited to the study of the evolution of male parental care. During mating, female syngnathids transfer eggs to specialized morphological structures that are located on either the abdomen or tail of the male. The male provides all postfertilization parental care and has morphological and physiological adaptations to osmoregulate, aerate, and even nourish the developing embryos. While all syngnathid species are adapted for paternal care, the brooding structure with which this is accomplished varies between species, from simple ventral gluing areas to much more complex structures such as the completely enclosed pouches of the seahorses. Our combined cytochrome b-, 12S rDNA-, and 16S rDNA-based molecular phylogeny of syngnathid fishes demonstrates that rapid diversification of male brooding structures has been associated with the major evolutionary radiation of the group, suggesting that development and diversification of structures involved in paternal care may have been key evolutionary innovations of the Syngnathidae. Molecular analyses also highlight geographical centers of biodiversity and suggest interoceanic migration of Syngnathus pipefishes from their center of origin in the Pacific.     

Sex differences in life history drive evolutionary transitions among maternal,paternal, and bi‐parental care

Evolutionary transitions among maternal, paternal, and bi‐parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life‐history characteristics (stage‐specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi‐parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi‐parental, bi‐parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex‐specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi‐parental → paternal, maternal → bi‐parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life‐history differences between the sexes can drive evolutionary transitions among different sex‐specific patterns of care. The finding that simple life‐history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter‐sexual life‐history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.     

Where are all the moms? External fertilization predicts the rise of male parental care in bony fishes

Parental care shows remarkable variation across the animal kingdom, but while maternal and biparental care are common in terrestrial organisms, male‐only care dominates in aquatic species that provide care. Using the most complete phylogenetic tree of bony fishes to date, we test whether the opportunity for external fertilization in aquatic environments can explain the more frequent evolution of male care in this group. We show that paternal care has evolved at least 30 times independently in fish and is found exclusively in externally fertilizing species. Male care is positively associated with pair spawning, suggesting that confidence in paternity is an important determinant of the evolution of care. Crucially, while female care is constrained by other forms of reproductive investment, male care occurs more frequently when females invest heavily in gamete production. Our results suggest that moving control of fertilization outside of the female reproductive tract raises male confidence in parentage and increases the potential for paternal care, highlighting that in an aquatic environment in which fertilization is external, paternal care is an effective reproductive strategy.     

Evolution of parental incubation behaviour in dinosaurs cannot be inferred from clutch mass in birds

A recent study proposed that incubation behaviour (i.e. type of parental care) in theropod dinosaurs can be inferred from an allometric analysis of clutch volume in extant birds. However, the study in question failed to account for factors known to affect egg and clutch size in living bird species. A new scaling analysis of avian clutch mass demonstrates that type of parental care cannot be distinguished by conventional allometry because of the confounding effects of phylogeny and hatchling maturity. Precociality of young but not paternal care in the theropod ancestors of birds is consistent with the available data.     

Differences in prolactin levels between three alternative male reproductive tactics in striped mice (Rhabdomys pumilio)

In male fishes, birds and mammals, increased prolactin secretion is thought to play a role in species showing paternal behaviours. This hypothesis was investigated in the striped mouse (Rhabdomys pumilio). This paper compares serum prolactin levels in 71 free-living male striped mice following three different reproductive tactics: (i) paternal group-living breeders, (ii) alloparental philopatric group-living males, and (iii) roaming non-paternal solitary males. Prolactin levels of breeding males were significantly higher than that of roamers. Alloparental philopatric males had low prolactin levels, which concur with studies of cooperatively breeding mammals, but contrasts with studies of cooperatively breeding birds. Both breeding males and females showed a decrease in prolactin levels after the breeding season, but not alloparental philopatric males. Prolactin levels were correlated with neither corticosterone levels nor age. These results are in agreement with the hypothesis that prolactin is one proximate mechanism of male reproductive tactics, possibly regulating differences in male parental care.     

The origin of parental care in relation to male and female life history

The evolution of maternal, paternal, and bi‐parental care has been the focus of a great deal of research. Males and females vary in basic life‐history characteristics (e.g., stage‐specific mortality, maturation) in ways that are unrelated to parental investment. Surprisingly, few studies have examined the effect of this variation in male and female life history on the evolution of care. Here, we use a theoretical approach to determine the sex‐specific life‐history characteristics that give rise to the origin of paternal, maternal, or bi‐parental care from an ancestral state of no care. Females initially invest more into each egg than males. Despite this inherent difference between the sexes, paternal, maternal, and bi‐parental care are equally likely when males and females are otherwise similar. Thus, sex differences in initial zygotic investment do not explain the origin of one pattern of care over another. However, sex differences in adult mortality, egg maturation rate, and juvenile survival affect the pattern of care that will be most likely to evolve. Maternal care is more likely if female adult mortality is high, whereas paternal care is more likely if male adult mortality is high. These findings suggest that basic life‐history differences between the sexes can alone explain the origin of maternal, paternal, and bi‐parental care. As a result, the influence of life‐history characteristics should be considered as a baseline scenario in studies examining the origin of care.     

Rapid allopatric speciation in logperch darters (Percidae: Percina)

Theory predicts that clades diversifying via sympatric speciation will exhibit high diversification rates. However, the expected rate of diversification in clades characterized by allopatric speciation is less clear. Previous studies have documented significantly higher speciation rates in freshwater fish clades diversifying via sympatric versus allopatric modes, leading to suggestions that the geographic pattern of speciation can be inferred solely from knowledge of the diversification rate. We tested this prediction using an example from darters, a clade of approximately 200 species of freshwater fishes endemic to eastern North America. A resolved phylogeny was generated using mitochondrial DNA gene sequences for logperches, a monophyletic group of darters composed of 10 recognized species. Divergence times among logperch species were estimated using a fossil calibrated molecular clock in centrarchid fishes, and diversification rates in logperches were estimated using several methods. Speciation events in logperches are recent, extending from 4.20 +/- 1.06 million years ago (mya) to 0.42 +/- 0.22 mya, with most speciation events occurring in the Pleistocene. Diversification rates are high in logperches, at some nodes exceeding rates reported for well-studied adaptive radiations such as Hawaiian silverswords. The geographic pattern of speciation in logperches was investigated by examining the relationship between degree of sympatry and the absolute age of the contrast, with the result that diversification in logperches appears allopatric. The very high diversification rate observed in the logperch phylogeny is more similar to freshwater fish clades thought to represent examples of sympatric speciation than to clades representing allopatric speciation. These results demonstrate that the geographic mode of speciation for a clade cannot be inferred from the diversification rate. The empirical observation of high diversification rates in logperches demonstrates that allopatric speciation can occur rapidly.     

Patterns of multiple paternity and maternity in fishes

The characterization of patterns of multiple mating is a major facet of molecular ecology and is paramount to understanding the evolution of behaviours associated with parental care and mate choice. Over the last 15 years, fishes have been particularly well studied with respect to multiple maternity and paternity thanks to the widespread application of microsatellite markers. The present review focusses on the impressive literature on genetic parentage in fishes. In studies of natural populations, we find that multiple paternity is extremely common across fish species, whereas rates of multiple maternity are much more variable. In species with nest defence, for example, rates of multiple maternity are strongly bimodal, and the occurrence of multiple dams per brood is either rare or the rule. The sex of the care‐giving parent is correlated with the rate of multiple parentage: when males provide uniparental care, rates of multiple paternity are low compared to rates of multiple maternity; when females provide parental care, either alone or assisted by males, rates of multiple paternity are highly variable, whereas rates of multiple maternity are quite low. These patterns may reflect conflicts between the reproductive interests of males and females. We also find that fishes in which females brood the offspring internally display much higher rates of multiple paternity compared to mammals or birds, whereas reptiles are intermediate. Male‐nesting fish species, however, show rates of multiple paternity more similar to those found in other vertebrates. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 735–760.     

Life history evolution in cichlids 1: revisiting the evolution of life histories in relation to parental care

Empirical links between egg size and duration of parental care in fishes have generated a considerable amount of theory concerning life history evolution. However, to date, this link has not been investigated in relation to other important life-history traits such as clutch size and body size, or while controlling for shared ancestry between species. We provide the first phylogenetically based tests using a database with information on egg size, clutch size, body size and care duration in cichlid fishes (Cichlidae). Multiple regression analyses, based on independent contrasts on both the species and the genus level, showed that clutch size is the variable most closely related to duration of care. This pattern appeared to be driven by post-hatch care relationships. Our results show that, contrary to expectation, there is no positive link between egg size and care duration in Cichlidae. Instead, greater reproductive output through increased clutch size investment appears to have coevolved with greater care of offspring. We suggest that re-evaluation of the generality of current models of the evolution of egg size under parental care in fishes is needed.     

Will male advertisement be a reliable indicator of paternal care,if offspring survival depends on male care?

Existing theory predicts that male signalling can be an unreliable indicator of paternal care, but assumes that males with high levels of mating success can have high current reproductive success, without providing any parental care. As a result, this theory does not hold for the many species where offspring survival depends on male parental care. We modelled male allocation of resources between advertisement and care for species with male care where males vary in quality, and the effect of care and advertisement on male fitness is multiplicative rather than additive. Our model predicts that males will allocate proportionally more of their resources to whichever trait (advertisement or paternal care) is more fitness limiting. In contrast to previous theory, we find that male advertisement is always a reliable indicator of paternal care and male phenotypic quality (e.g. males with higher levels of advertisement never allocate less to care than males with lower levels of advertisement). Our model shows that the predicted pattern of male allocation and the reliability of male signalling depend very strongly on whether paternal care is assumed to be necessary for offspring survival and how male care affects offspring survival and male fitness.     

LIFE HISTORY AND THE EVOLUTION OF PARENTAL CARE

Patterns of parental care are strikingly diverse in nature, and parental care is thought to have evolved repeatedly multiple times. Surprisingly, relatively little is known about the most general conditions that lead to the origin of parental care. Here, we use a theoretical approach to explore the basic life‐history conditions (i.e., stage‐specific mortality and maturation rates, reproductive rates) that are most likely to favor the evolution of some form of parental care from a state of no care. We focus on parental care of eggs and eggs and juveniles and consider varying magnitudes of the benefits of care. Our results suggest that parental care can evolve under a range of life‐history conditions, but in general will be most strongly favored when egg death rate in the absence of care is high, juvenile survival in the absence of care is low (for the scenario in which care extends into the juvenile stage), adult death rate is relatively high, egg maturation rate is low, and the duration of the juvenile stage is relatively short. Additionally, parental care has the potential to be favored at a broad range of adult reproductive rates. The relative importance of these life‐history conditions in favoring or limiting the evolution of care depends on the magnitude of the benefits of care, the relationship between initial egg allocation and subsequent offspring survival, and whether care extends into the juvenile stage. The results of our model provide a general set of predictions regarding when we would expect parental care to evolve from a state of no care, and in conjunction with other work on the topic, will enhance our understanding of the evolutionary dynamics of parental care and facilitate comparative analyses.     

A bibliography and categorization of bony fishes exhibiting parental care

Parental care occurs in a diversity of fishes, but predominantly among freshwater groups. Among the approximately 422 families of bony fishes (Osteichthyes), 89 are presently known to exhibit parental care. Grouping these families into eight categories, based on the sex of the care-giver(s), reveals male parental care is as common or more common than female parental care. Although unusual among vertebrates, parental care by males alone is very common among bony fishes. Lists of families, the forms of parental care exhibited, the modes of fertilization, the environments in which reproduction occurs, and the sources of documentation are presented. An extensive bibliography and index are provided.     

Evolution of paternal care in diploid and haplodiploid populations

W. D. Hamilton famously suggested that the inflated relatedness of full sisters under haplodiploidy explains why all workers in the social hymenoptera are female. This suggestion has not stood up to further theoretical scrutiny and is not empirically supported. Rather, it appears that altruistic sib‐rearing in the social hymenoptera is performed exclusively by females because this behaviour has its origins in parental care, which was performed exclusively by females in the ancestors of this insect group. However, haplodiploidy might still explain the sex of workers if this mode of inheritance has itself been responsible for the rarity of paternal care in this group. Here, we perform a theoretical kin selection analysis to investigate the evolution of paternal care in diploid and haplodiploid populations. We find that haplodiploidy may either inhibit or promote paternal care depending on model assumptions, but that under the most plausible scenarios it promotes – rather than inhibits – paternal care. Our analysis casts further doubt upon there being a causal link between haplodiploidy and eusociality.     

Effects of Exogenous Testosterone on Parental Care Behaviours in Male Bluegill Sunfish (Lepomis macrochirus)

Androgens are known to mediate aggressive and defensive behaviour in many vertebrate species. However, high concentrations of androgens might also conflict with the expression of nurturing behaviours and therefore a trade‐off can exist between aggressive and nurturing behaviours during parental care. We explored the role of testosterone in paternal care in bluegill sunfish (Lepomis macrochirus), where males provide both sole defence of the young from predators and sole nurturing behaviour such as fanning of the eggs. At the onset of parental care, we manipulated testosterone levels in males using testosterone propionate implants. We then observed the frequency of nurturing and aggressive behaviours displayed by the males over 6 d of parental care. Testosterone‐implanted fish were more aggressive when presented with a brood predator, performing more bites, opercular flares and lateral displays than control males. Testosterone‐implanted males, however, were not less nurturing than control fish, performing similar levels of fanning and nest‐cleaning behaviours. Thus, our results support a positive relationship between testosterone and paternal aggression but no testosterone‐mediated trade‐off between paternal nurturing and aggression.     

The unexpected but understandable dynamics of mating,paternity and paternal care in the ocellated wrasse

Although theory generally predicts that males should reduce paternal care in response to cues that predict increased sperm competition and decreased paternity, empirical patterns are equivocal. Some studies have found the predicted decrease in male care with increased sperm competition, while even more studies report no effect of paternity or sperm competition on male care. Here, we report the first example, to our knowledge, of paternal care increasing with the risk and intensity of sperm competition, in the ocellated wrasse (Symphodus ocellatus). Theory also predicts that if paternal care varies and is important to female fitness, female choice among males and male indicators traits of expected paternal care should evolve. Despite a non-random distribution of mating success among nests, we found no evidence for female choice among parental males. Finally, we document the highest published levels of extra-pair paternity for a species with exclusive and obligate male care: genetic paternity analyses revealed cuckoldry at 100 per cent of nests and 28 per cent of all offspring were not sired by the male caring for them. While not predicted by any existing theory, these unexpected reproductive patterns become understandable if we consider how male and female mating and parental care interact simultaneously in this and probably many other species.     

Effects of among-offspring relatedness on the origins and evolution of parental care and filial cannibalism

Parental care is expected to increase the likelihood of offspring survival at the cost of investment in future reproductive success. However, alternative parental behaviours, such as filial cannibalism, can decrease current reproductive success and consequently individual fitness. We evaluate the role of among-offspring relatedness on the evolution of parental care and filial cannibalism. Building on our previous work, we show how the evolution of care is influenced by the effect of among-offspring relatedness on both the strength of competition and filial cannibalism. When there is a positive relationship between among-offspring competition and relatedness, parental care will be favoured when among-offspring relatedness is relatively low, and the maintenance of both care and no-care strategies is expected. If the relationship between among-offspring competition and relatedness is negative, parental care is most strongly favoured when broods contain highly related offspring. Further, we highlight the range of conditions over which the level of this among-offspring relatedness can affect the co-occurrence of different care/no care and cannibalism/no cannibalism strategies. Coexistence of multiple strategies is independent of the effects of among-offspring relatedness on cannibalism but more likely when among-offspring relatedness and competition are positively associated.     

Sperm competition,sexual selection and the diverse reproductive biology of Osteoglossiformes

Osteoglossiformes are an order of “bony tongue” fish considered the most primitive living order of teleosts. This review seeks to consolidate known hypotheses and identify gaps in the literature regarding the adaptive significance of diverse reproductive traits and behaviour of osteoglossiforms within the context of sperm competition and the wider lens of sexual selection. Many of the unusual traits observed in osteoglossiforms indicate low levels of sperm competition; most species have unpaired gonads, and mormyroids are the only known vertebrate species with aflagellate sperm. Several osteoglossiform families have reproductive anatomy associated with internal fertilization but perform external fertilization, which may be representative of the evolutionary transition from external to internal fertilization and putative trade-offs between sperm competition and the environment. They also employ every type of parental care seen in vertebrates. Geographically widespread and basally situated within teleosts, osteoglossiforms present an effective study system for understanding how sperm competition and sexual selection have shaped the evolution of teleost reproductive behaviour, sperm and gonad morphology, fertilization strategies, courtship and paternal care, and sexual conflict. The authors suggest that the patterns seen in osteoglossiform reproduction are a microcosm of teleost reproductive diversity, potentially signifying the genetic plasticity that contributed to the adaptive radiation of teleost fishes.