Female Choice Predicts the Best Father in a Biparental Fish,the Midas Cichlid (Cichlasoma citrinellum)

The Midas cichlid is a monogamous, biparental species. It breeds in a highly competitive system where pairs have a low probability of raising fry to independence. Both parents must cooperate to retain the territory and protect the fry from predation. Previous experiments showed that females prefer large, aggressive and sexually experienced males as mates but males do not display any consistent preferences. Here I present the results of two experiments designed to see whether qualities preferred by females correlate with increased success in retaining territories and in providing parental care. Pairs with either large or aggressive males had an advantage in appropriating and holding a breeding territory; reproductive experience conferred no advantage in usurping a territory. Aggressive and reproductively experienced males had an advantage in defending the brood from predators of fry, but size had no effect. Thus, the qualities preferred by females confer advantages both in holding territories and in protecting fry. In contrast, males need not be selective because females, once in possession of a brood, defend it equally well regardless of size, aggressiveness, or reproductive experience. The system is one of mutually enforced monogamy based on female choice; females drive the system because they provide more investment than do males (combining gametes and time) and because this investment is a reliable resource to the male.     

Social Reversal of Sex‐Biased Aggression and Dominance in a Biparental Cichlid Fish (Julidochromis marlieri)

In biparental species, aggression, dominance, and parental care are typically sexually dimorphic. While behavioral dimorphism is often strongly linked to gonadal sex, the environment—either social or ecological—may also influence sex‐biased behavior. In the biparental cichlid fish Julidochromis marlieri, the typical social environment for breeding pairs consists of large females paired with smaller males. While both sexes are capable of providing territory defense and parental care, the larger female provides the majority of defense for the pair, while the smaller male remains in the nest guarding their offspring. We examine the contributions of sex and relative mate size to these sex‐biased behaviors in monogamous J. marlieri pairs. Both female‐larger and male‐larger pairs were formed in the laboratory and were observed for territorial aggression (against conspecifics and heterospecifics), dominance, and parental care. In female‐larger pairs, territorial aggression and intra‐pair dominance were female‐biased, while in male‐larger pairs this bias was reversed. For both pairing types, the presence of an intruder amplified sex differences in territorial aggression, with the larger fish always attacking with greater frequency than its mate. Though less robust, there was evidence for plasticity of sex‐bias for some egg care related behaviors in the inverse direction. Our study suggests that relative mate size strongly influences the sex bias of aggression and dominance in J. marlieri and that this aspect of the social environment can override the influence of gonadal sex on an individual's behavior. The remarkable plasticity of this species makes Julidochromis an exciting model that could be used to address the relationship between proximate and ultimate mechanisms of behavioral plasticity.     

Temporal and sex-specific patterns of breeding territory defense in a color-polymorphic cichlid fish

In biparental species, the costs and benefits of parental investment can vary between the sexes and shift over time. However, such sex-specific and temporal changes in territory defense are not well understood. Here, we experimentally investigated parental investment in breeding territory defense in a feral population of the color-polymorphic, biparental cichlid fish, the red devil (Amphilophus labiatus). We presented either gold- or dark-colored conspecific intruder models (i.e., dummy models) to A. labiatus pairs at three key stages during the breeding cycle (i.e., after pair formation, after eggs have been laid, and when fry were free-swimming). We found that males were more aggressive when the pair first formed, whereas females significantly increased their territory defense with time, and were most aggressive when fry were free-swimming. These results show that parental roles in territory defense can markedly shift over key stages of the breeding cycle. Our results demonstrate that parental behaviors may not only vary between the sexes, but can also shift dramatically over the course of the brood cycle.     

On the evolutionary pathway of parental care in mouth-brooding cichlid fishes

Evolutionary theory predicts that differences in parental care patterns among species arose from interspecific differences in the costs and benefits of care for each sex. In Galilee St Peter''s fish, Sarotherodon galilaeus (Cichlidae), male care, female care and biparental care all occur in the same population. We exploit this unusual variability to isolate conditions favouring biparental versus uniparental mouth-brooding by males or females. We first review a game-theoretic model of parental care evolution, predictions of which we test experimentally in this paper. Manipulations of the operational sex ratio show that males and females desert their offspring more frequently when the costs of care are high (in terms of lost mating opportunities). Breeding trials with males of different sizes show that small fathers desert more frequently than large fathers. We attribute this to the associated difference in the fitness benefit of biparental care relative to female-only care. Our experimental results confirm that in St Peter''s fish the probability of caring is determined facultatively according to current conditions at each spawn. The experiments and model together suggest that interspecific variation in remating opportunities and clutch size may be responsible for differences in care patterns within the sub-family Tilapiini. Our results support the hypothesis that biparental mouth-brooding was the ancestral state of both male and female uniparental mouth-brooding in cichlid fishes.     

Social Monogamy in the Big-Clawed Snapping Shrimp, Alpheus heterochelis

Social monogamy has evolved independently in many taxa, and often involves biparental care of the young. Where it does not, mate guarding and shared territoriality have been invoked as causal factors. We evaluated mate guarding and shared resource defence (a common shelter) as factors that could have led to social monogamy in the snapping shrimp, Alpheus heterochelis. This species is found in male–female pairs that defend a common shelter together. Female receptivity lasts only for a few hours immediately after her periodic moult. Their monogamous pair bond may represent mate guarding or joint defence of a territory. Monogamy in A. heterochelis seems most importantly driven by the cryptic nature of the female's moult cycle. We found that males did not discriminate among females at different intermoult stages for pairing, nor did they modulate their defence of mate and shelter (vs. the risk in finding a new shelter and mate) according to female moult stage. This, together with the short period of female receptivity before her single copulation per cycle, make extended mate guarding the most efficient method for a male to secure a mating opportunity. Comparing eviction rates of paired and unpaired shelter residents by conspecific intruders provided no evidence of enhanced resource defence that would confer a selective advantage to a pair. Male presence during the moult is beneficial for the female, as searching for a male during her soft-bodied receptive phase would put her at mortal risk. Our results show empirically for the first time that guarding may be beneficial, even if males are not able to assess the female's reproductive stage. This extends the theoretical framework for understanding the evolution of social monogamy in taxa without biparental care of young.     

Sexual-Selection Models for Exaggerated Traits are Useful but Constraining

SYNOPSIS. Science is driven by productive hypotheses and technology,but these may sometimes limit the questions posed. For instance,Fisherian runaway sexual selection and related hypotheses havehelped us understand the evolution of exaggerated visual sexualdimorphism. Species with indistinguishable sexes, however, mayuse different behavioral mechanisms when pairing and thus possessdifferent adaptations. In the monomorphic Midas cichlid (Amphilophuscitrinellum), females chose large aggressive males in a restrainedsituation, as sexual selection predicts, but males did not choose.The nuchal hump of males swells coincidently with pair formation.However, overly large humps were shunned by females while thenormal— size hump facilitated sex recognition. This speciesis polychromatic, and pairs mate assortatively by color in Nicaragua.Some have suggested the Midas cichlid might therefore show howsexual selection produces explosive speciation of cichlids inAfrica. All females, however, are biased toward normal—colormales. The color of gold morphs modulates aggressive responsesof the other fish. All else equal, the benefit to gold in afight equals 15% more weight than the opponent. Pair formationsucceeds best when the typically smaller female of a pair isrelatively more aggressive than the male. The pair combination,gold male with normal female, is difficult to produce; makingthe female the same size as the male removes the disability.Pair formation is a negotiated process in which the male teststhe aggressiveness of the female relative to self. That putsthe behavioral mechanisms of the male and female in conflict.     

The reproductive biology of a Central American cichlid Neetroplus nematopus in Lake Xiloá,Nicaragua

This study was conducted to provide a five-year database on the breeding seasonality and breeding biology of a Central American cichlid fish Neetroplus nematopus, a biparental substratum-spawning cichlid that cares for its eggs, wrigglers, and fry for up to six weeks. A total of 503 breeding pairs were monitored for breeding success. Breeding pairs of N. nematopus are sexually dimorphic in size, with females averaging 39% of male body mass. Fry emerged from 85% of nesting cavities. After three weeks, only 30% of the broods were present in the nesting cavity; these broods had a 30% survival rate, giving a 9% overall survival rate. Nineteen percent of the successful parents with three-week-old broods adopted foreign fry. A consistent unimodal breeding peak in December was observed for five years. This breeding peak differed dramatically from the bimodal breeding season 20 years found in the 1970s. The effects of extensive grenade fishing practices during the 1980s might have played a substantial role in the observed change. Grenade fishing stopped in 1991, and the number of N. nematopus pairs increased by 136% from 1990 to 1995. With increased density of breeding fish, the breeding season for this species also expanded. The balance between divergent selection due to competition for breeding sites and stabilizing selection due to predation pressure on offspring is of breeding is a strategy to reduce predation on the parent's own young [Current Zoology 56 (1): 43-51 2010].     

Effect of Mate Removal on Current and Subsequent Parental Care in the Convict Cichlid (Pisces: Cichlidae)

In most biparental, substrate-brooding species of cichlid fishes, female and male roles differ. Females are usually more involved in direct care of the young while males spend more time away patrolling the territory. This study tested the flexibility of these sex roles with removal experiments in the convict cichlid, Cichlasoma nigrofasciatum. When males were removed, female fanning activity increased. When females were removed, males spent more time fanning and less time away from the brood. Other behavioural variables (frequency of digging, mouthing, foraging and retrieving) were not affected. Being alone or paired during a first breeding episode did not affect parental behaviour during a subsequent episode in which all fish were paired. Observations were carried out during the day and at night, and nocturnal fanning of fry is reported here for the first time. Female role appears less flexible than male role, as befits the more direct care normally given by females.     

Mating behavior of Pine Sawyer,Monochamus saltuarius Gebler (Coleoptera: Cerambycidae)

Mating behavior of the pine sawyer, Monochamus saltuarius Gebier (Cerambycidae: Lamiinae) was observed on pine trees in an outdoor net cage kept in one healthy pine tree and a cluster of pinelogs (cut over one month) to attract the beetles. When sawyer adult pairs released into net cage, they all moved to the pinelogs. And then the male was staying motionless with his antenna outstretched while the female was actively moving in his vicinity. The mating behavioral reactions were followed by the next steps: The first phase of courtship was initiated by the female approach toward the male. Second, male dashed, contacted antenna and mounted female's back. Third, female carried the male on her back and walked around and then male began to lick. Fourth, male inserted his penis into the female's genitalia when female stopped walking. While a long pairbond, the mating pair repeated copulations, lastly, when mating is over, male and female stayed separately. The mating began on sunset and resting of both male and female began at the temperature below about 20 °C. Substantially straightforward mate searching by female indicates the presence of a male sex pheromone.     

Factors affecting mate desertion by males in free-ranging convict cichlids (Cichlasoma nigrofasciatum)

Convict cichlid fish have biparental care for a period of about6 weeks lasting from egg laying until the young (fry) have grownto about 10 mm. However, the young can sometimes survive withcare from only one parent, and desertion of the mate and offspringby males has been observed. I tested a theoretical model modifiedfrom Lazarus (1990) which predicted that mate and offspringdesertion by male convict cichlids should be promoted by lowpredation pressure on fry, high remating opportunities for males,increasing age of fry, and decreasing number of fry. Males deserted7.8% of 334 broods studied during two breeding seasons in CostaRican streams. As predicted, males deserted their broods mostfrequently at sites with the highest brood survivorship (lowestbrood predation pressure), when fry were close to independenceand when brood size was smaller than average. Sex ratios andinterspawning intervals did not indicate any relationship betweenmate desertion and opportunities for remating for males. Thereuse of spawning caves may favor fidelity to the mate and brood,and defending the young from predators at the same time as defendingthe cave from conspecifics may favor biparental care in thisspecies.     

How Similar is the Coordination of Parental Roles Among Different Pairs? An Examination of a Monogamous Fish

Although most studies on biparental care assume that parents cooperate in raising offspring, few studies have documented how parents coordinate their activities. Using the biparental convict cichlid (Archocentrus nigrofasciatum) we compared the parental behavior of both single (‘widowed’) parents and individuals within pairs during the 5 d when the offspring were in the relatively uniform and stationary wriggler stage. In particular, we were interested in the consistency of day‐to‐day parental activities among single individuals and among individuals within pairs. Single parents showed differences in most parental activities that were consistent from one day to the next. This day‐to‐day consistency remained after an intruder was added and / or the mate was present. Thus, although the social context changed (i.e., presence or absence of mate, presence or absence of an intruder), an individual's consistency remained. The male and female within pairs were significantly correlated in the time spent on most parental activities across experimental pairs. Thus, while individuals within pairs were unique in their performance of a parental activity, paired males and females managed a high degree of correlation (i.e., coordination). In general, pairs were homogeneous in the degree to which males and females were correlated across different parental activities.     

The effect of partial brood loss on male desertion in a cichlid fish: an experimental test

There is little experimental evidence testing whether currentbrood size and past brood mortality influence mate desertion.In the cichlid Aequidens coeruleopunctatus both parents initiallydefend offspring. In a field study, all experimental broods,irrespective of initial brood size (222.9 ± 60.4, mean± SD), were manipulated to a size of 100 fry. Neitherthe duration nor investment of females in parental care differed between control and brood reduced pairs, even though care seemedcostly. On average, females lost 5.1 ± 4.8% of initialweight while guarding a brood until independence. In contrast,males with experimentally reduced broods guarded fry for significantlyfewer days before deserting their mate than did males fromcontrol pairs with natural-sized broods (20.5 ± 7.5 vs. 14.2 ± 6.2 days). In at least 20% of cases (n = 9/45),the deserting male immediately mated with another female. Maleswith experimentally reduced broods also spent less time guardingfry before deserting and attacked fewer brood predators thandid males with control broods. For broods manipulated to have100 fry, there was a significant negative relationship betweenthe days until male desertion and the proportion of the initialbrood removed. This indicates that male assessment of the futuresuccess of the current brood (hence its reproductive value)is based on past mortality and/or that there is variation amongmales in the expected size of future broods. Both current broodsize and brood size relative to initial brood size are thereforepredictors of male, but not female, parental behavior and matedesertion. Female care may be unaffected by brood reductiondue to limited breeding opportunities and partial compensationfor reduced male care.     

Differences in Aggressiveness in the Midas Cichlid Fish (Cichlasoma citrinellum) in Relation to Sex,Reproductive State and the Individual

The Midas cichlid, Cichlasoma citrinellum, is monogamous and biparental. Because of competition for limited spawning sites and intense predation on their young, vigorous defense of their territory is essential. Although both sexes engage in defense, they differ in aggressiveness. The aggressive responses of both sexes were measured by counting the number of bites and bumps each fish directed toward its own mirror image. The size of the fish's genital papilla was also recorded to estimate its reproductive state. Compared with females, males had higher median mirror scores with greater variance. The scores of individual males were also more consistent through time than were those of females. Females close to spawning had the highest mirror scores, whereas male scores were highest early in the reproductive cycle. Selection has apparently favored aggressiveness in both sexes. We argue, however, that differences in aggression are the result of selection acting dissimilarly on the two sexes.     

Parental care and mating systems of cichlid fishes in Lake Tanganyika: a preliminary field survey

Reproductive ecology and ethology of 52 cichlid fishes were studied along the shore of Myako, east-middle coast of Lake Tanganyika. Seventeen species were substrate-brooders (guarders), 31 were mouthbrooders, and the remaining 4 were intermediate, performing prolonged biparental guarding of fry after mouthbrooding. Among the substrate-brooders maternal care (and polygyny) was seen about as frequently as biparental care. In most of the mouthbrooders only females took care of the brood, but in 3 species eggs and small larvae were mouthbrooded by females and larger fry by males. In most of the maternal mouthbrooders males defended mating territories which females visited to spawn. The mating system differed from lekking in that there was no concentration of territories and males fed within them. In the remaining maternal mouthbrooders males and overlapping home ranges and only temporarily defended courtship sites in each bout of spawning. Brood size, egg size, breeding site, and sexual differences in body size and color are described. The relationship between parentalcare patterns and mating systems within the family Cichlidae are discussed.     

The effects of mate separation on pair re-formation in the Texas cichlid fish (Cichlasoma cyanoguttatum)

This study tested whether mated pairs of Texas cichlid ($\text{Cichlasoma cyanoquttatum}$) would reform and continue rearing their offspring after being separated for either one, four, or ten days. All pairs successfully re-formed after one day, while only 50% re-formed after 4 days. No pair re-formed after 10 days of separation. In successfully re-formed pairs, the female was always more aggressive than her mate, irrespective of whether the female was the resident or the returning individual. Aggressiveness seemed related to the female's attempt to control the male's parental behavior. For pairs which did not re-form, the resident parent, either the male or female, violently and continously attacked the returned mate.     

Intraspecific brood adoption in the convict cichlid with respect to fry of two colour morphs

Convict cichlid Cichlasoma nigrofasciatum adults of the melanistic morph usually accepted fry of the same colour morph provided these were of approximately the same age and size as those of the receiver pair, whereas older and considerably younger fry were rejected or eaten. Xanthoric fry were usually accepted and rejected to the same extent as fry of their own colour morph. However, in certain combinations, especially when alien fry were 3 weeks old and the adopting parents already had their own 2 week old fry, fry of their own colour morph were significantly more likely to be adopted.     

Is Mating Different in Monogamous Species? The Midas Cichlid Fish as a Case Study

Monogamous species are typically sexually isomorphic, pair wellbefore spawning is imminent, take much time to pair, are discerningabout pairing, and appear to weigh multiple sources of informationabout species, sex, and quality of mate. The monogamous andpolychromatic Midas cichlid (Cichlasoma citrinellum) distinguishedbetween its own and a highly similar heterospecific behind aone-way mirror only when visual and chemical cues matched. Likewise,recognition of sex was hindered when interaction was precluded,even in the presence of chemical cues. Female choice of matewas most strongly influenced by the "normal, " primitive, colorand to a lesser degree by color of parents and siblings, makingit difficult to account for positive color-assortative matingin the field. Females also selected the largest and the mostaggressive males; size predicted a good defender of territory,and aggressiveness foretold effective protection of the young.Males, however, were not choosy. Pair formation features muchaggression between the large male and smaller female, and gold-coloredmorphs (G) dominate normal (N) ones. That made it difficultfor an N female to pair with a G male; using an N female thesame size as the G male, however, resulted in the usual proportionof successful pairings. I propose three testable models of paircompatibility: complementarity, parity, and maximum male aggressiveness.     

Polymorphic microsatellite loci optimised for studies on the convict cichlid fish (<Emphasis Type="Italic">Amatitlania siquia</Emphasis>)

The neotropical convict cichlid fish (Amatitlania siquia) is an important model species for the study of animal behaviour. It is therefore surprising that no genetic markers are available for this species. Here, we have optimised four polymorphic microsatellite loci for use with this fish, where each locus comprises between 9 and 28 alleles. We demonstrate how these markers can be used to genotype fry (young) and for the analyses of genetic structure and prevalence of interfamilial mixing within biparental broods of wild convict cichlids. These microsatellites will facilitate future research, hitherto not possible, on the molecular, behavioural and evolutionary ecology of the convict cichlid and possibly other closely related species.