Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird

The greater ani (Crotophaga major), a Neotropical cuckoo, exhibits an unusual breeding system in which several socially monogamous pairs lay eggs in a single nest and contribute care to the communal clutch. Cooperative nesting is costly-females compete for reproduction by ejecting each other's eggs-but the potential direct or indirect fitness benefits that might accrue to group members have not been identified. In this study, I used molecular genotyping to quantify patterns of genetic relatedness and individual reproductive success within social groups in a single colour-banded population. Microsatellite analysis of 122 individuals in 49 groups revealed that group members are not genetic relatives. Group size was strongly correlated with individual reproductive success: solitary pairs were extremely rare and never successful, and nests attended by two pairs were significantly more likely to be depredated than were nests attended by three pairs. Egg loss, a consequence of reproductive competition, was greater in large groups and disproportionately affected females that initiated laying. However, early-laying females compensated for egg losses by laying larger clutches, and female group members switched positions in the laying order across nesting attempts. The greater ani, therefore, appears to be one of the few species in which cooperative breeding among unrelated individuals is favoured by direct, shared benefits that outweigh the substantial costs of reproductive competition.     

Dispersal in Kin Coalition Throughout the Non‐Breeding Season to Facilitate Fine‐Scale Genetic Structure in the Breeding Season: Evidence From a Small Passerine

Evidence shows that social cooperation among kin may evolve even in birds with extensive dispersal. In such cases, maintaining kinship during dispersal is essential to the subsequent expression of kin cooperation. This hypothesis has not been examined for most bird species. We addressed it in the ground tit (Parus humilis), a passerine where kin frequently interact in terms of cooperative polygamy and extra‐pair mating despite fast annual turnover of the breeding population. Pedigree and genotype data showed that while groups varied in composition throughout the non‐breeding season due to continual individual emigration and immigration, they always contained kin coalitions consisting of either local or immigrant individuals of different age and sexes. The first‐order kin coalitions, according to the information from local individuals, stemmed from single‐family lineages (siblings and their parents), and the lower‐order ones from neighbouring, related family lineages that merged after fledging. It was probable that immigrants had formed kin coalitions in similar ways before dispersing. Groups broke up in the breeding season. Pairing between unrelated individuals from different coalitions within a group was more likely, whereas related individuals from the same coalition tended to nest near each other. The resulting fine‐scale population genetic structure is expected to facilitate breeding interactions among kin. Our findings give clues to understanding the evolution of social cooperation in relation to dispersal.     

Genetic structure, relatedness and helping behaviour in the yellow mongoose in a farmland and a natural habitat

The yellow mongoose Cynictis penicillata is a facultatively social species and provides an opportunity to study the evolution of social behaviour. We examined genetic structure, relatedness and helping behaviour in the yellow mongoose in natural habitat in the Kalahari Desert, where the species lives in small family groups of up to four individuals and shows no cooperative breeding; and in farmland in the Western Cape Province of South Africa, where they live in larger groups of up to 13 individuals, engage in numerous social interactions and show cooperative breeding. The farmland population showed significant inbreeding, and lower genetic variability than the desert population, but there was no evidence of a recent population bottleneck. The genetic relatedness between individuals within social groups and that between future potential helpers and pups were higher in the farmland population than in the desert population. However, based on a limited sample, helping effort (in the farmland population) was not preferentially directed towards kin. Thus, the origin of helping in the farmland population is consistent with kin selection, but in the absence of kin discrimination, future research should investigate whether long-term breeding opportunities or group augmentation contribute to maintaining cooperative breeding in this population.     

Evolutionary routes to non-kin cooperative breeding in birds

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection—when individuals increase their inclusive fitness by aiding genetic relatives—is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.     

The utility of AFLPs for supporting mitochondrial DNA phylogeographical analyses in the Taiwanese bamboo viper, Trimeresurus stejnegeri

An amplified fragment length polymorphism (AFLP) assay was performed on individuals representing discrete haplotypes from two genetically distinct mtDNA lineages of the bamboo viper, Trimeresurus stejnegeri (Schmidt), within Taiwan. AFLP (525 polymorphic markers from five primer pairs) and mtDNA genetic distances were highly correlated and an analysis of molecular variance, and a Bayesian approach similarly partitioned estimates of genetic similarity according to the mtDNA phylogeographical pattern. These results are discussed in relation to biogeographical hypotheses, comparative rates of mtDNA molecular evolution, and in the identification of evolutionary significant units of Taiwanese T. stejnegeri. In spite of the high degree of congruence between the genetic datasets, the AFLP phylogenetic analysis did not support the mtDNA tree, suggesting that no contemporary barriers to gene flow exist between individuals from the two mtDNA lineages.     

Development of microsatellite markers in the grey‐crowned babbler (Pomatostomus temporalis)

The grey‐crowned babbler (Pomatostomus temporalis) is a cooperative breeding bird species in which nonbreeding helpers of both sexes care for the young of breeding individuals. To measure the genetic relatedness between breeders and their offspring and helpers, we developed nine microsatellite markers. Most of the loci were highly polymorphic. These loci will be useful in understanding the evolution and maintenance of cooperative breeding and helping behaviour in this species.     

Introgression of mitochondrial DNA among lineages in a hybridogenetic ant

We report a remarkable pattern of incongruence between nuclear and mitochondrial variations in a social insect, the desert ant Cataglyphis hispanica. This species reproduces by social hybridogenesis. In all populations, two distinct genetic lineages coexist; non-reproductive workers develop from hybrid crosses between the lineages, whereas reproductive offspring (males and new queens) are typically produced asexually by parthenogenesis. Genetic analyses based on nuclear markers revealed that the two lineages remain highly differentiated despite constant hybridization for worker production. Here, we show that, in contrast with nuclear DNA, mitochondrial DNA (mtDNA) does not recover the two lineages as monophyletic. Rather, mitochondrial haplotypes cluster according to their geographical origin. We argue that this cytonuclear incongruence stems from introgression of mtDNA among lineages, and review the mechanisms likely to explain this pattern under social hybridogenesis.     

Homogeneity and distinctiveness of Polish paternal lineages revealed by Y chromosome microsatellite haplotype analysis

Different regional populations from Poland were studied in order to assess the genetic heterogeneity within Poland, investigate the genetic relationships with other European populations and provide a population-specific reference database for anthropological and forensic studies. Nine Y-chromosomal microsatellites were analysed in a total of 919 unrelated males from six regions of Poland and in 1,273 male individuals from nine other European populations. AMOVA revealed that all of the molecular variation in the Polish dataset is due to variation within populations, and no variation was detected among populations of different regions of Poland. However, in the non-Polish European dataset 9.3% ( P<0.0001) of the total variation was due to differences among populations. Consequently, differences in R(ST)-values between all possible pairs of Polish populations were not statistically significant, whereas significant differences were observed in nearly all comparisons of Polish and non-Polish European populations. Phylogenetic analyses demonstrated tight clustering of Polish populations separated from non-Polish groups. Population clustering based on Y-STR haplotypes generally correlates well with the geography and history of the region. Thus, our data are consistent with the assumption of homogeneity of present-day paternal lineages within Poland and their distinctiveness from other parts of Europe, at least in respect to their Y-STR haplotypes. Electronic supplementary material to this paper can be obtained by using the Springer LINK server located at http://dx.doi.org/10.1007/s00439-002-0728-0.     

The influence of maternal lineages on social affiliations among humpback whales (Megaptera novaeangliae) on their feeding grounds in the southern gulf of Maine

Humpback whales on their feeding grounds in the Gulf of Maine typically form fluid fission/fusion groups of two to three individuals characterized by noncompetitive and, at times, cooperative behavior. Here we test the hypothesis that, despite the apparent absence of close kinship bonds, the fluid associations between feeding whales are influenced by "maternal lineages" as represented by mtDNA haplotypes. Using skin samples collected with a biopsy dart, variation in the hypervariable segment of the mtDNA control region identified 17 unique haplotypes among 159 individually identified whales from the southern Gulf of Maine. The haplotypes of a further 143 individuals were inferred from known direct maternal (cow-calf) relationships. The frequencies of associations among these 302 individuals were calculated from 21,617 sighting records collected from 1980 to 1995, excluding associations between a cow and her dependent calf. For groups of two where the haplotypes of both individuals were known (n = 3,151), individuals with the same haplotype were together significantly more often (26%) than expected by random association (20%). To account for different group sizes and associations with individuals of unknown haplotype and sex, we used Monte Carlo simulations to test for nonrandom associations in the full data set, as well as known female-only (n = 1,512), male-only (n = 730), and mixed-sex (n = 2,745) groups. Within-haplotype associations were significantly more frequent than expected at random for all groups (P = .002) and female-only groups (P = .011) but not male-only groups, while mixed-sex groups approached significance (P = .062). A Mantel test of individual pairwise association indices and haplotype identity confirmed that within-haplotype associations were more frequent than expected for all sex combinations except male-male associations, with females forming within-haplotype associations 1.7 times more often than expected by random assortment. Partial matrix correlations and permutation analyses indicated that the skew toward within-haplotype associations could not be accounted for by short-term temporal co-occurrence or fine-scale spatial distributions of individuals with shared haplotypes. While the mechanism by which individuals with a common mtDNA haplotype assort remains unknown, our results strongly suggest an influence of maternal lineages on the social organization of humpback whales within a regional feeding ground.     

Changes in genetic diversity and differentiation in Red‐cockaded woodpeckers (Dryobates borealis) over the past century

Red‐cockaded woodpeckers (RCW; Dryobates borealis) declined after human activities reduced their fire‐maintained pine ecosystem to <3% of its historical range in the southeastern United States and degraded remaining habitat. An estimated 1.6 million RCW cooperative breeding groups declined to about 3,500 groups with no more than 10,000 birds by 1978. Management has increased RCW population abundances since they were at their lowest in the 1990s. However, no range‐wide study has been undertaken since then to investigate the impacts of this massive bottleneck or infer the effects of conservation management and recent demographic recoveries. We used mitochondrial DNA sequences (mtDNA) and nine nuclear microsatellite loci to determine if range‐wide demographic declines resulted in changes to genetic structure and diversity in RCW by comparing samples collected before 1970 (mtDNA data only), between 1992 and 1995 (mtDNA and microsatellites), and between 2010 and 2014 (mtDNA and microsatellites). We show that genetic diversity has been lost as detected by a reduction in the number of mitochondrial haplotypes. This reduction was apparent in comparisons of pre‐1970 mtDNA data with data from the 1992–1995 and 2010–2014 time points, with no change between the latter two time points in mtDNA and microsatellite analyses. The mtDNA data also revealed increases in range‐wide genetic differentiation, with a genetically panmictic population present throughout the southeastern United States in the pre‐1970s data and subsequent development of genetic structure that has remained unchanged since the 1990s. Genetic structure was also uncovered with the microsatellite data, which like the mtDNA data showed little change between the 1992–1995 and 2010–2014 data sets. Temporal haplotype networks revealed a consistent, star‐like phylogeny, suggesting that despite the overall loss of haplotypes, no phylogenetically distinct mtDNA lineages were lost when the population declined. Our results may suggest that management during the last two decades has prevented additional losses of genetic diversity.     

Helper effects in the azure‐winged magpie Cyanopica cyana in relation to highly‐clumped nesting pattern and high frequency of conspecific nest‐raiding

In avian cooperative breeding systems, many benefits obtained by social pairs from the presence of helpers have been uncovered. However, until now, the factors that determine the type of assistance helpers provide and the responses of social pairs have not been well illustrated. We examined the contribution of helpers to cooperative groups and the relevant responses of dominant pairs in the azure‐winged magpie Cyanapica cyana which breeds on the Tibetan Plateau. We used the capture–mark–recapture method to identify helpers. Results showed that helpers were mostly the yearling sons of dominant pairs. They mainly contributed to the cooperative group in three ways, courtship‐feeding the incubation female, provisioning the brood, and defending the nest. For responses of dominant pairs, we unexpectedly found that clutch size was not influenced by the presence of helpers at the nest. However, cooperative groups had higher brood feeding rates than biparental nests and their feeding pattern also differed to that of the latter. Consequently, nestlings in cooperative groups had larger fledging body mass than that in biparental nests. By examining reasons for nest failure, we revealed that conspecific nest‐raiding contributed to more nest failure than any other natural predators. Because of the contribution of helpers in defending against both predators and conspecific nest‐raiders, cooperative groups had higher survival rate than biparental nests. Thus, our findings suggest that in a highly‐clumped nesting pattern, factors concerning the risk of nest predation, rather than that influencing food supply, play an important role in determining helper effects and responses of aided dominant pairs.     

Enhanced phylogeographic information about Austrian brown trout populations derived from complete mitochondrial control region sequences

Complete DNA sequences of the control region revealed a more fine-scale genetic structuring within and among Austrian brown trout Salmo trutta populations providing the opportunity for gene frequency analyses in the phylogeographic context. Ninety-two individuals (75%) were assigned to nine Danubian haplotypes and 31 individuals (25%) comprised seven Atlantic haplotypes of northern European origin. Three of the Atlantic haplotypes were also found in an Austrian hatchery breeding stock.     

Great bustard population structure in central Spain: concordant results from genetic analysis and dispersal study.

We found significant sex differences in the mtDNA genetic structure and dispersal patterns of great bustards in a population of 11 breeding groups, "leks", in central Spain. The analysis of genetic distances showed that the female population was divided into three groups of leks separated by ca. 50 km, whereas male haplotypes were randomly distributed among leks. Genetic distances among pairs of leks were positively correlated with geographical distances in females but not in males. While female haplotype distributions were homogeneous among leks at close distances, differences in male genetic structure were highly variable even between two close leks. These results from genetic analyses were concordant with those from a radiotracking study on natal dispersal. Natal dispersal distances were higher in males than in females. Also, the frequency of movement of a female between two leks was positively correlated with their genetic affinity and geographical proximity. In males, the frequency of movement was correlated with geographical proximity but not with genetic affinity. Males dispersed among genetically unrelated leks, contributing to keep nuclear genetic diversity in the population, whereas females tended to be philopatric. These results suggest that isolation-by-distance influences the distribution of maternal lineages at a regional level.     

Composition of native and introduced mtDNA lineages in <Emphasis Type="Italic">Coregonus</Emphasis> sp. in two Austrian lakes: evidence for spatio-temporal segregation of larvae?

We hypothesized that there is spatio-temporal genetic (mtDNA) structure of native and introduced larval whitefish (Coregonus sp.) in two Austrian lakes (Traunsee and Hallstättersee). Larval whitefish were sampled from 12 sites in each lake and screened for variation in the mtDNA NADH-1 gene. Based on the sequencing of adult fish together with existing GenBank sequences, an RFLP protocol was developed to assign haplotypes from larval samples into one of two divergent lineages. All but one site (pelagic) in Traunsee contained both haplotypes, thus there was no support for spatial segregation of mtDNA groups in that lake. However, weekly sampling from December to May in Traunsee revealed a temporal pattern, with the native haplotypes dominating in December and January before the appearance of the introduced Baltic clade. In Hallstättersee, only three of the 12 sites sampled revealed haplotypes from the introduced clade and thus spatial segregation seems operative on that lake. Our results imply that differences in the spawning ecology of the two groups maintain sufficient reproductive isolation to be reflected in distinct larval occurrence in space and time highly consistent with genetic differences on the mtDNA level. If the two lineages were highly introgressed, we would expect to find little or no correspondence between spatio-temporal patterns in larval distribution and the differentiated mtDNA lineages.     

Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds

In cooperatively breeding species, restricted dispersal of offspring leads to clustering of closely related individuals, increasing the potential both for indirect genetic benefits and inbreeding costs. In apostlebirds (Struthidea cinerea), philopatry by both sexes results in the formation of large (up to 17 birds), predominantly sedentary breeding groups that remain stable throughout the year. We examined patterns of relatedness and fine-scale genetic structure within a population of apostlebirds using six polymorphic microsatellite loci. We found evidence of fine-scale genetic structure within the study population that is consistent with behavioural observations of short-distance dispersal, natal philopatry by both sexes and restricted movement of breeding groups between seasons. Global F(ST) values among breeding groups were significantly positive, and the average level of pairwise relatedness was significantly higher for individuals within groups than between groups. For individuals from different breeding groups, geographical distance was negatively correlated with pairwise relatedness and positively correlated with pairwise F(ST). However, when each sex was examined separately, this pattern was significant only among males, suggesting that females may disperse over longer distances. We discuss the potential for kin selection to influence the evolution and maintenance of cooperative breeding in apostlebirds. Our results demonstrate that spatial genetic structural analysis offers a useful alternative to field observations in examining dispersal patterns of cooperative breeders.     

Group structure,within-group conflict and reproductive tactics in cooperatively breeding Galápagos mockingbirds,Nesomimus parvulus

Reproductive conflict within groups can be an important feature of cooperative breeding systems, especially when more than one individual of a sex breeds within a social group. Relationships between group structure, dominance, within-group conflict and reproductive tactics of cooperatively breeding Galápagos mockingbirds were examined on Isla Genovesa. Territorial groups of 2–24 adults included up to three breeding females, with 42% of the groups containing more than one (plural groups); females in most plural groups nested separately. Territory size increased with group size, but the area available per pair in plural groups was smaller than in singular groups (groups with only one breeding pair). Most pairings were monogamous, and males usually outnumbered females; high-ranking males obtained mates more frequently than subordinate males. In 3 relatively dry years, but not in a wet El Niño year, subordinate pairs in plural groups fledged fewer young than dominant pairs or pairs breeding in singular groups. Interference by dominant breeders, often leading to abandonment of nests by subordinate pairs, appears to account for these differences: through nest disruption in drier years, dominant individuals may reduce the cost of sharing their territories and increase the chances of recruiting helpers. Dominant males in plural groups may also father young through extra-pair copulations with subordinate females. Despite costs imposed by within-group conflict, subordinate breeders have higher long-term reproductive success than birds that defer breeding. Plural group structure is maintained because unpredictable climatic variation favours opportunistic breeding by subordinates.     

Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys

The cooperatively breeding bell miner, Manorina melanophrys, differs from most other cooperative breeding species in the complexity of its social system, where discrete social organization occurs on at least three levels. Microsatellite markers were used to investigate the degree of genetic structure underlying the social organization of M. melanophrys by comparing colonies, coteries and nest contingents. The genetic data confirmed behavioural observations of M. melanophrys living in male kin-based groups between which females disperse short distances to breed. Estimates of FST revealed restricted gene flow between eight colonies located within 30 km that was significantly associated with geographical distance when the two most distant colonies were included. Within a high density colony significant differences were found between coteries; analysis of the degree of relatedness between coterie members showed that this is due to related individuals associating preferentially with each other. Similarly, the contingent of individuals attending a nest were generally close relatives of the young they were aiding, supporting models invoking kin selection as the selective agency mediating helping.     

Genetic structure analysis of mantis shrimp <Emphasis Type="Italic">Oratosquilla oratoria</Emphasis> based on mitochondrial DNA control region sequence

The genetic relationships of mantis shrimp Oratosquilla oratoria between the coastal waters of China and Japan were not well studied. To reveal the genetic differentiation and genetic structure among populations, we collected populations of mantis shrimp O. oratoria from the coastal waters of China and Japan to analyze the mtDNA control region variation. A total of 309 individuals of O. oratoria were collected from 13 localities (11 from China and 2 from Japan) and a segment of mitochondrial DNA control region was sequenced. Three hundred nine haplotypes were defined, yielding a very high haplotype diversity and nucleotide diversity. Two lineages of O. oratoria were revealed and displayed strong differences in the geographical distribution. In the coastal waters of China, the geographic distribution of the two lineages was completely separated by the Yangtze River estuary; however, the lineages showed geographic sympatry in two populations from Japan. Based on the lineage distribution, three groups were defined. There was no significant genetic differentiation among the populations within the three groups, indicating high gene flow within each group. Significant and negative values for Tajima D and Fu’s Fs tests, and mismatch distributions for two lineages indicated population expansion. The present result confirmed that the freshwater outflow from the Yangtze River formed a physical barrier and affected gene exchange. The different distribution patterns of the two lineages in coastal waters of China and Japan indicated that the larvae of O. oratoria were transferred from China to the coastal waters of Japan with a one-way gene flow.     

Molecular Phylogeny and Genetic Divergence of the Introduced Populations of Japanese Guppies, Poecilia reticulata

A phylogenetic tree of guppies from seven introduced Japanese populations was constructed using a mitochondrial gene, and the relationship between these Japanese populations and indigenous South American populations was examined. Phylogenetic trees constructed by maximum parsimony and neighbor joining methods indicated four major groups: Group A: Trinidadian populations; Group B: the northernmost Okinawa populations; Group C: the northern Okinawa populations; Group D: Shimoda populations and the remainder of Trinidadian, Venezuelan, and southern Okinawa populations. Considerable genetic differences were observed among the haplotypes within each Okinawa population similar to that found among haplotypes of different native populations, but not within the Shimoda population, because each Okinawa population included haplotypes belonging to different groups. Genetic differences between Groups B, C, and D might reflect those of the introduced lineages; however, these differences might not result from the divergence after introduction events. These results suggested that multiple introductions of different breeding lineages might cause considerable divergence within and between Okinawa populations.     

New insights into the intraspecific cytoplasmic DNA diversity,maternal lineages classification and conservation issues of Tunisian pearl millet landraces

Tunisian pearl millet (Pennisetum glaucum L.) landraces are still growing in contrasting agro-ecological environments and are considered potentially useful for national and international breeders. Despite its genetic potential, the cropping areas of this species are still limited and scattered which increases the risk of genetic erosion. The chloroplast DNA polymorphism and maternal lineages classification of forty nine pearl millet landraces representing seven populations covering the main distribution area of this crop in Tunisia were undertaken based on informative cpSSR molecular markers. A total of 21 alleles combining to 9 haplotypes were detected with a mean value of 3.5 alleles per locus and a haplotype genetic diversity (Hd) of 0.82. The number of chloroplast haplotypes per population ranged from 1 to 4 with an average of 1.28. The haplotypes median-joining network and UPGMA analyses revealed two probable ancestral maternal lineages with a differential pearl millet seed-exchange rate between the investigated areas. Northern and Central populations presented unique genetic backgrounds while historical farmers’ practices in the South-East area resulted in the isolation of their own local landraces. The genetic evidences strongly support at least two introduction origins of pearl millet in Tunisia, one in the North and the other in the South followed by distinct local dispersal histories. Complementary in-situ and ex-situ conservation strategies taking into account the conservation of the maternal lineage cytoplasmic diversity are required. The investigated chloroplast SSRs provide useful molecular markers which could be used in further genetic studies and breeding surveys of pearl millet genetic resources.