Egg mimicry and allopaternal care: two mate-attracting tactics by which nesting striped darter (Etheostoma virgatum) males enhance reproductive success

In a variety of fish species with paternal care of offspring, females prefer to spawn in nests that already contain eggs. This female preference has been hypothesized to explain egg thievery in male sticklebacks, allopaternal care of eggs in minnows, and the evolution of egg-mimicking body features in male cichlids and darters. Here we employ microsatellite-based parentage analyses to evaluate the reproductive success of striped darter (Etheostoma virgatum) males that appear to utilize two of these functionally related tactics to entice females to spawn in their nests. In an isolated population (Clear Creek, Ky.), we observed that breeding males develop conspicuous white spots on their pectoral fins. If these spots are egg mimics, as we suspect, then this represents the fourth independent evolutionary origin of egg mimicry documented to date in darters, the first based on pigmentation (as opposed to physical structures), and the first in which the egg mimics vary greatly in number among males. From direct counts of microsatellite genotypes in clutches of embryos, at least 3.8 females contributed to the progeny within a typical nest, and females tended to spawn preferentially with males that were larger and displayed more egg-mimic spots. In another population (Hurricane Creek, Tenn.) without egg mimics, the multi-locus genetic data document that allopaternal care is common, especially among the smallest males who sometimes tend nests containing their own as well as an earlier sire's offspring. Thus, these foster males had adopted egg-containing nests and then successfully spawned with subsequent females. Overall, the genetic data on paternity and maternity, in conjunction with field observations, suggest that egg mimicry and allopaternal care are two mate-attracting reproductive tactics employed by striped darter males to exploit female preferences for spawning in nests with 'eggs'. Electronic Publication     

Male–male competition and alternative male mating tactics influence female behavior and fertility in Japanese medaka (Oryzias latipes)

Intense male–male competition driven by high male density during mating can result in the evolution of alternative mating tactics that increase male fertilization success. The effects of alternative male mating tactics on females can range from increased fertilization and genetic benefits to decreased fertilization and loss of paternal care. However, the influence of male competitive behavior and alternative mating tactics on female behavior and reproductive success has seldom been addressed. In this work, I investigated the occurrence of alternative male mating tactics and their potential influence on female behavior and fertilization success in Japanese medaka (Oryzias latipes). Groups of one, two, or four males competed for access to a female in a repeated-measures experiment. Male density had a significant influence on female reproductive output as a result of a change in competitive mode from contest to scramble competition that coincided with more disruption during mating when more than one male attempted to mate. By contrast, sneaking during mating was beneficial to males, as more than one male sired offspring in most spawnings involving sneaker males. These results suggest that there may be conflict between males and females over mating, such that females are detrimentally affected by the occurrence of alternative mating tactics, whereas males may benefit from sneak mating. The occurrence of conflict between the sexes can be related to ecological factors, such as male density, which cause behavioral change in both males and females.     

Sex and status in a cooperative breeding fish: behavior and androgens

Among taxonomically widespread cooperatively breeding vertebrates, those with non-breeding helpers-at-the-nest provide an excellent opportunity to understand the proximate mechanisms underlying care and allocare. In this study, we examined androgen levels in relation to care behavior in a cooperatively breeding cichlid fish, Neolamprologus pulcher, from Lake Tanganyika. We concentrated on androgens, as these hormones have been linked to the defense behavior, and the defense of young is a common form of parental care in fishes. N. pulcher dominant female breeders performed the most care and also displayed the highest levels of plasma testosterone (T) compared with other individuals within the social group. We also found that dominant male breeders provided a similar amount of care as did the subordinate helpers, but breeding males had the highest levels of 11-ketotestosterone (11KT), an important androgen in fish. Breeders had higher levels of both androgens (T and 11KT) compared to helpers. There was a weak but significant positive correlation between T levels and the frequency of care regardless of sex and status. Our results suggest that androgens may promote defense of young and are in contrast to the commonly reported trade-off between androgen and parental care.     

Indiscriminate care of offspring predates the evolution of sociality in alloparenting social spiders

Alloparental care—the care of other’s offspring—is a key aspect of sociality in many groups of animals. Understanding how this complex behavior arises requires identifying both the selective forces that may favor it, as well as characteristics of particular lineages that facilitate or hinder its evolution. One potential hindrance is the existence of discrimination against foreign offspring, an obstacle that would need to be overcome in order for alloparental care to evolve. In this study, we explored whether offspring discrimination may have constrained the evolution of alloparental care in social spiders in the genus Anelosimus. Social spiders are known for their cooperative behaviors, which include alloparental care. After quantitatively assessing the extent of alloparenting in the care of egg sacs in natural nests of these spiders, we investigated whether discrimination against foreign egg sacs existed in ancestral pre-social species in the genus. We did so by testing for discrimination between a female’s own and foreign egg sacs in three subsocial sister taxa of each social species investigated. We found no detectable evidence of discrimination in the care of egg sacs by female Anelosimus, regardless of level of sociality. We used these data, along with those from previous studies, to infer that a lack of discrimination is likely the ancestral state in the genus Anelosimus. This supports the idea that offspring discrimination was not a constraint on the evolution of alloparental care in social Anelosimus species. We discuss the evolutionary implications of this finding, and suggest that lack of offspring discrimination may have eased the transition from solitary to cooperative breeding.     

Brood defense and filial cannibalism in the spottail darter (<Emphasis Type="Italic">Etheostoma squamiceps)</Emphasis>: the effects of parental status and prior experience

Male spottail darters (Etheostoma squamiceps) defend nest sites in which females deposit eggs over the course of several weeks. In laboratory experiments, I tested three predictions of the hypothesis that the presence of eggs increases the value of a nest site to male spottail darters: (1) males should preferentially defend nests with eggs over empty nests, and males that sired the eggs should (2) spend more time defending them and (3) consume less of their broods than should alloparent males. Parent males were tested using eggs they were guarding in the field; alloparents included males that were not defending eggs immediately prior to the experiment (inexperienced), and males that were defending eggs in the field when captured but were given eggs sired by a different male (experienced). In choice experiments in which males were offered nest sites differing only in the presence of eggs, males preferred to defend nest sites with eggs regardless of parental status. Parent males spent significantly more time defending eggs and consumed less of their broods than did inexperienced alloparent males. Experienced alloparent males were similar to parent males in brood defense but had levels of filial cannibalism similar to inexperienced males, suggesting that prior experience may influence brood defense but not egg consumption.     

Male spottail darters (Etheostoma squamiceps) do not use chemical or positional cues to discriminate between sired and foster eggs

Filial cannibalism is hypothesized to allow nest-guarding males to recoup energy lost during nest defense. Males in many species of fishes occasionally defend broods containing both sired and foster eggs due to shifts in nest site ownership or cuckoldry. Such males are predicted to consume primarily foster eggs if the ability to discriminate among eggs exists. In a previous laboratory study, male spottail darters (Etheostoma squamiceps) consumed significantly more foster eggs than sired eggs, suggesting the existence of a mechanism for discrimination using chemical or positional cues. This discrimination mechanism in the spottail darter was tested by creating nest sites with half sired eggs and half foster eggs (n=15), or with all sired eggs with half positionally relocated (n=9). Males defended these nests for 2 days in the field, and cannibalism was determined by counting eggs lost during that interval. Neither foster eggs nor relocated sired eggs were consumed in greater numbers or percentages of the original brood sizes than the unchanged sired eggs, indicating that male spottail darters do not discriminate between foster and sired eggs by olfaction or position. Alternatively, the hypothesis that males treat all eggs in nest sites in which they have spawned as sired explains the results of both studies.     

Pup guarding by greater spear-nosed bats

Alloparental care poses an evolutionary dilemma because effort is expended on non-filial offspring. Thus, instances of alloparental care have been attributed to either mistaken identity, (i.e., recognition errors) or active cooperation. In greater spear-nosed bats (Phyllostomus hastatus), reproductive females roost together in stable long-term social groups in cave ceilings. Non-volant pups frequently fall from roost sites to the cave floor where they can die unless retrieved by an adult. In this study, we examined the function of adult female visits to non-filial young and tested whether visits were attributable to recognition errors or to cooperation. We found that females visited non-filial pups from their own social group more than expected. Females from different social groups attacked and sometimes killed pups, and male pups were attacked more frequently than female pups. Visits by group mates benefited fallen pups by reducing the likelihood of attack by females from other groups. In contrast to the mistaken identity hypothesis, we found that some females leave their own pups to approach and remain with group mates’ pups. We used microsatellite markers to estimate relatedness and test whether kinship could explain this alloparental care and found that females were unrelated to the pups they guard. We conclude that females who reside in highly stable social groups exhibit cooperative behavior that cannot be explained by kinship and is unlikely to be due to direct or generalized reciprocity. Instead, our data suggest that alloparental care likely involves a complex interplay between group membership and cooperative foraging.     

Dominance and reproductive behavior of wild house mice in a seminatural environment correlated with T-locus genotype

Summary Behavior of mice whose T-locus genotype was either +/+ or +/t was observed in a seminatural environment. Heterozygous females were less likely to be dominant, less likely to go into behavioral estrus, and less likely to become pregnant than were +/+ females. The relative fitness of +/t as compared with +/+ females was 0.32:1.00. In contrast, +/t males produced 35% more young than did +/+ males. The higher fitness of +/t males was primarily due to a greater production of young on the part of +/t as compared with +/+ subordinate males. Little evidence was found under these naturalistic conditions, of non-random mating with respect to T-locus genotype. The indication of overdominance for +/t males makes it unlikely that heterozygote disadvantage will be sufficient to account for the frequency of t-alleles in natural populations.     

Egg-mimicry as a mating strategy in the fantail darter,Etheostoma flabellare: females prefer males with eggs

Summary In some species of fishes with paternal care, females prefer to spawn with males already defending eggs. Such female preference appears to have resulted in adoption of unrelated eggs as a male mating strategy in several species. Page and Swofford (1984) proposed that such female preference may have also resulted in the evolution of male egg-mimics in several species of darters (Percidae); however, their hypothesis has not been tested. We examined female preference in the fantail darter (Etheostoma flabellare) and found that females preferred males with eggs over males without eggs, and males with egg-mimics over males without egg-mimics. Thus it appears that female preference for males already guarding eggs may have led to the evolution of specialized egg-mimicking morphology in males.     

Providing parental care entails variable mating opportunity costs for male Temminck’s stints

Males of many species theoretically face a fitness tradeoff between mating and parental effort, but quantification of this is rare. We estimated the magnitude of the mating opportunity cost paid by incubating male Temminck’s stints (Calidris temminckii), taking advantage of uniparental care provided by both sexes in this species. “Incubating males” provide all care for an early clutch, limiting subsequent mating possibilities. “Non-incubating” males include males that failed to obtain, lost to predation, or actively avoided incubating clutches. These males were free to pursue extrapair copulations and to mate with females laying later clutches, which females usually incubate themselves. Male incubation classes did not differ in measures of quality, and many individuals changed classes between years, suggesting the use of conditional reproductive tactics. However, specialist non-incubators may also exist. Using microsatellites to assign parentage, we compare males’ total fertilizations and the subset “free of care” fertilizations between incubation classes. Incubators were more likely to gain at least one fertilization per season and averaged one more per season than non-incubators. However, successful non-incubators were more likely to gain “free of care” fertilizations, averaging two more than successful incubators. The relative success of male incubation classes also changed with local sex ratios. With higher female proportions, non-incubators gained disproportionately more offspring, suggesting that the use of tactics should be partly determined by the availability of potentially incubating females. Overall, we estimate the opportunity cost of incubating to be 13–25 % of the potential annual reproductive output.     

Behavioral strategies of American kestrels during mate replacement

Summary To determine the influence of mate replacement on the behavior and reproductive success of wild American kestrels (Falco sparverius) we removed 4 female and 16 male members of breeding pairs during incubation in 1983 and 1984. Eight males and 1 female were replaced within a mean time of 43 h. Widowed females that received a replacement spent less time hunting, but incubated and performed aerial displays more frequently than females that did not receive a replacement. After replacement, widowed females continued to incubate the original clutch, yet copulated and performed other courtship behaviors with the incoming male. Overlapping of normal temporally separate behavioral cues may be a female strategy to gain assistance from a replacement mate. However, none of the original clutches was successfully hatched. Of 8 pairs with replacement males, 2 pairs abandoned their territory, two remained on territory but did not renest, and 4 renested within a mean interval of 18 days. The lone female replacement and her mate copulated and performed nest inspections but then abandoned the territory. Incubation behavior was similar between replacement and control pairs; however, replacement males fed more invertebrate prey to nestling and made many more nest visits. All 3 replacement nests that hatched young failed within 8 days.     

Role of female territoriality in social and mating systems of Canthigaster valentini (Pisces: Tetraodontidae): evidence from field experiments

Sharpnose puffers, Canthigaster valentini (Pisces: Tetraodontidae) at Lizard Island, Australia, live in made-dominated haremic social and mating systems. The hypothesis was that mature females are restricted in their movements and can be monopolized by some males. Field experiments at Lizard Island, Great Barrier Reef, between January and March 1983 showed that mature females were still territorial in the absence of males and movements of females were not controlled by males. Males abandoned their territories when their females were removed. The territorial behavior of those males with access to females (territorial males) restricted the access of other males (bachelor males) to them. Bachelor males took over harems and became territorial males when established territorial males were removed. The results of the experiments thus supported the hypothesis.     

Chemosensory cues allow male lizards<Emphasis Type="Italic"> Psammodromus algirus</Emphasis> to override visual concealment of sexual identity by satellite males

Males of many species of lizards show conspicuous breeding colors but, in some species, young competitively inferior males conceal their sexual identity by a female-like dull coloration that allows them to evade aggression from dominant males and to adopt an alternative satellite-sneaking mating tactic. However, large males of the lizard Psammodromus algirus reacted aggressively to young intruder males despite their female-like coloration, suggesting that they might have the ability to recognize competitor males by chemosensory cues. We experimentally manipulated the head coloration (brown vs orange) and scents (male vs female) of small young males. For staged agonistic encounters, we compared the response of resident unmanipulated large males to the different manipulated small males. When we manipulated only the color of small males, the response of resident large males was independent of the paint manipulation; brown and orange males elicited a similar aggressive response. However, when we also manipulated the scent, small males painted orange or brown, but bearing the scent of males, received a significantly higher number of aggressive responses than small males painted orange or brown, but bearing the scent of females. The results showed that, at close range, the reaction of large males to manipulated individuals was dependent on the scent, whereas color seemed to be less important. Coloration may be, however, more important in long-distance communication as shown by the outcome of the first encounters. Also, orange coloration may increase the intensity of the aggressive response. Effective sex recognition by territorial large males is important in natural situations to avoid sneak matings by young male competitors. Thus, even if small males visually conceal their sexual identity, chemosensory cues allow large males to identify them at close range.     

Does the cost of polygyny in house wrens include reduced male assistance in defending offspring?

Summary This study investigated whether reduced male aid in defending offspring potentially reduces the fitness of females choosing already-mated males in the house wren (Troglodytes aedon), a small, territorial songbird. Frozen snakes were placed at 23 nests of monogamously mated males and 12 secondary nests of bigamously mated males. All presentations were made during incubation stages of females attending focal nests. Snakes were placed at nests of secondary females when nests of their primary counterparts contained young 5–9 days old. Males are most attentive to primary nests during this period and should therefore be relatively inattentive to secondary mates and nests. Nevertheless, an equal proportion of monogamous and bigamous males discovered snakes within 15 min, and mean time to discovery, when discovery occurred, did not differ with nest status. Monogamous and bigamous males were also equally likely to attack snakes physically once discovered. Monogamous males appeared no more likely to discover snakes than bigamous males for two main reasons. First, although monogamous males were near focal nests (i.e., < 10 m) more often than bigamous males, monogamous males tended to stay out of view of nests for long periods. In contrast, bigamous males always went immediately to focal nests upon arriving in their vicinity. Second, about one-third of monogamous males in this study spent much of their time during trials at the far edges of their territories advertising for secondary mates. Our experiment suggests that reduced male aid in defending nests against small, diurnal predators probably does not contribute to the cost of polygyny in house wrens. Correspondence to: L.S. Johnson     

Offspring recognition and the influence of clutch size on nest fostering among male sand gobies, Pomatoschistus minutus

When parental care is costly, parents should avoid caring for unrelated young. Therefore, it is an advantage to discriminate between related and unrelated offspring so that parents can make informed decisions about parental care. In the present study, we test the hypothesis that male sand gobies (Pomatoschistus minutus) recognize and differentially care for their own offspring when given a choice between a nest with sired eggs and a second nest with eggs sired by an unrelated male. The sand goby is a species with exclusive and costly paternal care. Male parasitic spawnings (e.g., sneaking) as well as nest takeovers by other males are common. Our results show that nests containing sired eggs were preferred and received significantly more care, as measured by nest building and nest occupancy, than nests with foreign eggs even when males cared for both nests. These findings suggest that males respond to paternity cues and recognize their own clutches. Relative clutch size also had a significant effect on male parental care. When sired clutches were larger than foreign clutches, males preferred to care for their own nest. In the few cases where males chose to take care of foreign nests, the foreign clutch was larger than their own clutch. Taken together, our results provide evidence that both paternity cues and clutch size influence parenting decisions among male sand gobies.     

Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor

For males of socially polygynous avian species like the spotless starling, there may exist a trade-off between investing in paternal care and controlling several nests. To determine how the intensity of paternal care affects reproductive success per brood sired or expressed as the total number of young raised in all nests controlled by the same male, it is necessary to manipulate paternal care. Testosterone (T) has been shown to depress the tendency for males to care for their young, and induces them to acquire more mates. The effects of paternal care on reproductive success were studied by treating certain male starlings with exogenous T and others with the antiandrogen cyproterone acetate (CA), and comparing the parental behavior of T- and CA-males throughout the breeding season with that of controls. CA-males fed their chicks more during the first week after hatching than T-males, with controls feeding at intermediate rates, both on a per nest basis and as total effort for all nests controlled by the same male. Paternal feeding rates during the first week of chick life had a significant positive effect on the number of fledged young. The hormone treatment significantly affected the number of chicks raised per nest, CA-males having a higher breeding success per nest than T-males, and controls showing intermediate levels of success. There was no significant effect of treatment on total reproductive success attained by males throughout the season. In the polygonous spotless starling, the intensity of paternal care of young affects reproductive success per nest positively but not on a seasonal basis. Received: 6 February 1999 / Received in revised form: 30 June 1999 / Accepted: 11 July 1999     

Breeding success of a brood parasite is associated with social mating status of its host

Reproductive success of brood parasites varies considerably both among and within host species, mainly due to differences in host egg-rejection rates and survival of parasitic chicks. Here, we investigated the breeding success of the cuckoo (Cuculus canorus) in one of its major hosts, the great reed warbler (Acrocephalus arundinaceus), with respect to host social mating status. In this passerine, polygynous males provide less parental care to their young per nest than monogamous males. Consequently, their less-assisted females may fledge lower numbers of nestlings than monogamous females. This may be especially true for secondary females, which often receive limited or no paternal help with young at all. Based on these findings, we expected higher cuckoo reproductive success in nests of socially monogamous than polygynous great reed warbler males. More specifically, we predicted lower fledging success of cuckoo young in nests of secondary than primary or monogamous females. In line with the prediction, we found higher cuckoo fledging success in nests of monogamous than polygynous males, monogamous nests being more than twice as successful as secondary nests. We detected, however, only a tendency to lower cuckoo success in primary compared to monogamous nests and no differences between primary and secondary nests. Moreover, neither parasitism nor host egg-rejection rates differed among the nests of different status. Our results show, for the first time, that the social mating status of a host may influence the overall reproductive success of a brood parasite and thus should be considered in further studies.     

Female control of reproductive skew in cooperatively breeding brown jays (<Emphasis Type="Italic">Cyanocorax morio</Emphasis>)

Brown jays (Cyanocorax morio) are long-lived, social corvids that live in large, stable, territorial groups (mean = 10 individuals). In this study, I determined the distribution of reproductive success within groups using multi-locus DNA fingerprinting. Breeding females produced virtually all (99%) of the young within their own nests. Reproduction within groups was highly skewed towards a single primary female, although long term data indicate that secondary females (female breeders that were usually younger and subordinate to the primary female) were sometimes successful. The high reproductive skew observed for females was associated with primary female aggression. Successful reproduction by secondary females may have been due to parental facilitation or the inability of primary females to completely suppress secondary females. Multiple paternity occurred in 31–43% of broods and extra-group paternity occurred in a minimum of 22% of broods. Patterns of paternity also varied between years, since females often switched or included new genetic mates. Although male consorts of nesting females fathered relatively few offspring (20%), they still had a higher chance of fathering offspring than any other single group male. Reproduction was less skewed for males than females as a result of female mating patterns. Female reproductive patterns are consistent with some of the predictions and assumptions from optimal skew models, while male reproductive patterns are not. The factors affecting skew in species with complex social systems such as incomplete control by breeders over subordinate reproduction, female control of paternity, and resource inheritance have not been well incorporated into reproductive skew models.Communicated by: J. Dickinson     

Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus)

In males of socially monogamous birds, plasma testosterone (T) typically declines to low levels during the parental phase. Studies on multiple-brooded species indicate that high T may be incompatible with high-quality paternal care. The length of the breeding season may affect the costs and benefits of high T and its effect on paternal care. We studied the effect of experimentally elevated T on paternal care in a single-brooded species with a short breeding season, the Lapland longspur (Calcarius lapponicus). We monitored T levels and parental behavior in 16 males with subcutaneous T implants, 14 males with empty implants, and 14 unimplanted males. We videotaped nests when nestlings were 2–3 days old and again at 4–5 days. T males with 2- to 3-day-old young visited nests and fed young less often than control males, and the mates of the T males compensated with elevated visits and feedings. However, when nestlings were 4–5 days old, T males visited their nests at normal rates – though feeding movements remained below normal – and T females visited and fed at normal rates. Nestling mass and nest success were similar in both groups. Overall, high T suppresses paternal care in Lapland longspur males. The partial improvement of paternal care when nestlings are older, despite high T, may be related to the short 6-week breeding season of this arctic species, and the consequently reduced benefits of sexual behavior late in the breeding season. Received: 2 February 1998 / Accepted after revision: 2 November 1998     

Helping at the nest,allofeeding and social status in immature arabian babblers

Summary Arabian babblers, Turdoides sqamiceps, are cooperatively breeding, group territorial birds, occurring in desert habitats. Non-breeders participate in several types of cooperative behaviour, including care of eggs, nestlings and fledglings, and bringing food to one another (allofeeding). This paper reports on observations of helping with eggs and young, and peer allofeeding, performed by immature babblers, fledged the previous season or earlier in the same season. The birds were from a babbler population studied since 1971 in the Arava valley of eastern Israel. They belonged to groups in which all individuals had been colourringed and were accustomed to human observers. Individuals and nests in the territories of these groups could be watched from distances of 1–2 m without causing alarm, so fine details of behaviour could be observed in the field. In most allofeeding interactions observed, a more dominant individual brought food to a subordinate. Sometimes the subordinate bird avoided accepting the proferred food, and was then hit or chased by the bird that had attempted to feed it. Occasionally a subordinate bird attempted to feed a more dominant individual. Dominant birds always refused to take food offered by a subordinate, and hit or chased any subordinate attempting to feed them. Frequencies of visits to nests were correlated with helper rank for those visits where the incoming bird displaced a previous visiter from the nest. Frequences of visits to unattended nests, however, were not correlated with helper rank. Similarly, frequencies of feeding visits to fledglings were correlated with helper rank until incubation of the next brood began. After this, the correlation disappeared. Numerous instances of aborted nest visits were observed in which a helper, often carrying food, arrived at the nest-tree but left again without visiting the nest. In many other cases, a helper arrived at the nest-tree but delayed visiting the nest for several minutes. Aborted and delayed visits usually occurred when a more dominant bird was in the vicinity of the nest. This suggests interference between helpers. Direct interference between helpers visiting fledglings was occasionally observed. In such cases, a more dominant helper snatched food from a subordinate approaching fledglings, and then fed this food to the fledglings itself. Interference between helpers, and conflict between proferers and recipients of food during allofeeding, are not easily explained by kin selection or reciprocity. On the other hand, such behaviour is readily explained by a hypothesis which suggests that individuals may increase their social status in the group by performing cooperative behaviour. Babblers that establish status by demonstrating ability to bear the short-term costs of cooperative behaviour, rather than through direct aggression towards rivals, are likely to forge collaborative relationships with other group members. Since babblers must collaborate to establish and defend a territory, such relationships are essential to reproductive success.