Susan B. McRae

Intraspecific brood parasitism in the moorhen : parentage and parasite-host relationships determined by DNA fingerprinting

Abstract Parasitic female moorhens (Gallinula chloropus) lay from one to six eggs in the nests of conspecific neighbours. DNA fingerprinting was used to show that parasitic eggs could be correctly identified when they appeared in addition to or outside the host’s laying sequence. Moorhen hosts accept all parasitic eggs laid after the 2nd day of their laying period. To understand why moorhen hosts tolerate parasitic eggs, we tested two hypotheses. (1) The quasi-parasitism hypothesis: females lay their eggs in the evening when the host males are normally in attendance at the nest, so host males may allow parasitic females to lay in their nests in exchange for fertilizing their eggs. However, DNA fingerprinting showed that all the parasitic eggs were sired by the parasites’ mates. Parasitic moorhens frequently continue laying a clutch in their own nest, without a break in the laying sequence after a parasitic laying bout. The eggs laid by brood parasites in their own nests were also sired by their own mates. Therefore this hypothesis was rejected. (2) The kin selection hypothesis: if one or both members of the host pair are close relatives of the parasite, the costs of rearing parasitic chicks will be to some degree offset by inclusive fitness benefits. We examined the genetic relationships between parasites and their hosts using DNA fingerprinting and genealogical data. Natal philopatry by both sexes was relatively common in this population, and the probability that a neighbour of either sex was a first-order relative (parent-offspring) was calculated as 0.18. Although first-order relatives were not preferentially chosen as hosts over individuals that were not first-order relatives, even through random host selection there is almost a one-in-five chance that brood parasites in this population are closely related to their hosts. This may facilitate host tolerance of parasitic eggs. Other hypotheses are also discussed.

A dominant allele controls development into female mimic male and diminutive female ruffs

Maintaining polymorphisms for genes with effects of ecological significance may involve conflicting selection in males and females. We present data from a captive population of ruffs (Philomachus pugnax) showing that a dominant allele controls development into both small, ‘female mimic’ males (‘faeders’), and a previously undescribed class of small ‘female faeders’. Most male ruffs have elaborate breeding plumage and display behaviour, but 0.5–1.5% are faeders, which lack both. Females from a captive population previously lacking faeders were bred with two founder faeder males and their faeder sons. The faeders’ offspring had a quadrimodal size distribution comprising normal-sized males and females, faeders and atypically small females. By contrast, ornamented males fathered only normal-sized offspring. We conclude that both founding faeders were heterozygous for a faeder allele absent from the original population. This allele is dominant to previously described genes that determine development into independent versus satellite ornamented males. Unlike those genes, the faeder allele is clearly expressed in females. Small body size is a component of the male faeder mating strategy, but provides no obvious benefit to females. Bisexual expression of the gene provides the opportunity to quantify the strength of sexually antagonistic selection on a Mendelian trait.

Can incest within cooperative breeding groups be detected using DNA fingerprinting

Although generally considered a rare phenomenon, in-cest has been observed in a number of populations ofbirds and mammals in which dispersal is limited (Green-wood et al. 1978; Bulger and Hamilton 1988; Gibbs andGrant 1989; Packer and Pusey 1993; Keller and Arcese1998). In cooperatively breeding animals where off-spring remain in their natal territory as adults, the oppor-tunity for incest may be substantial (Ligon and Ligon1990). Inbreeding avoidance mechanisms ensure thatcases of incest in the cooperatively breeding acornwoodpecker (Melanerpes formicivorus) are exceedinglyrare, and groups whose membership consists of onlyclosely related members of the opposite sex may foregobreeding for up to 3 years if membership remains unal-tered (Koenig et al. 1998). Incest is avoided in the su-perb fairy wrenMalurus cyaneusthrough a differentmechanism: although offspring remain on their natal ter-ritory, females seek extra-group matings, particularlywhen many sons remain as helpers in the group (Brookeret al. 1990; Mulder et al. 1994). Few other studies of co-operatively breeding populations have verified genetical-ly whether or not incest occurs.To date, most studies that have looked at genetic rela-tionships within groups of cooperatively breeding ani-mals have used multilocus DNA fingerprinting (Rabenoldet al. 1990; Jones et al. 1991; Packer et al. 1991; Bruce etal. 1996; Whittingham et al. 1997; Lundy et al. 1998). Inseveral cases, the authors appear not to have appreciatedthat this technique does not allow the detection of parent-offspring incest. While some have acknowledged the lim-itations of the data and were careful not to make inferenc-es beyond the scope of the technique (Haig et al. 1994;Dickinson et al. 1995; McRae 1996; Koenig et al. 1998),others have simply ignored the possibility of incest. Sincegenetic data of this nature are often compiled to drawgeneral conclusions about levels of reproductive skew(Reeve and Keller 1995), and inbreeding (Heinsohn et al.1990; Pusey and Wolf 1996), it is important that this pos-sibility is not overlooked. We outline here why conven-tional DNA fingerprinting is limited, and in some casesunsuitable, for studying parentage in social animals, anddiscuss the power of typing with microsatellite markers.The technique of multilocus DNA fingerprinting suf-fers from the constraint that individual bands cannot beassigned to known loci making it impossible to deter-mine whether a given band is of paternal or maternal ori-gin (Jones et al. 1991; McRae 1996; Danforth andFreeman-Gallant 1996). Careful analyses are required todetermine whether or not bands are segregating indepen-dently. For example, bands may be consistently scoredtogether (linkage), or they may appear mutually exclu-sive (allelism). Although segregation analyses can beused to calculate the probability of error due to non-inde-pendence, this is not always helpful for parentage analy-sis when parental candidates are the first-order relativesof other parental candidates.Paternity analysis with multilocus DNA fingerprintsrelies on the existence of ‘diagnostic’ bands to excludeindividuals from parentage. The problem with analyzingfingerprints of cooperative groups arises uniquely whenthere is an adult helper in the group that is the full off-spring of the dominant pair. This is a very commongroup structure among avian cooperative breeders re-ferred to as ‘simple’ family groups (Emlen 1995). Takethe example of a dominant pair whose adult son remainsin the group as a helper. When a chick is the offspring ofthe dominant male and female (i.e., the full sibling of thehelper), assuming the identity of the mother is reliable,there will often be (paternal) bands found in the finger-prints of the chick and the dominant male that are notfound in that of the helper son. Thus it is usually possi-ble to exclude the son from paternity. However, if achick is the product of mother-son incest, it is impossibleto exclude the dominant male (i.e., the actual grandfather

Why some rails have white tails: the evolution of white undertail plumage and anti-predator signaling

Conspicuous plumage patches have evolved in birds as conspecific signals for mate attraction and assessment, intersexual competition or to signal alarm. Signals may alternatively be directed at potential predators to discourage pursuit. Rails (Family Rallidae) are ground-dwelling birds, many of which inhabit wetlands, while others occur in forests and grasslands. They are renown for their secretive nature and the tendency to flick their tails when observed. This behavior is more conspicuous in species with white undertail coverts that contrast sharply with darker body plumage. Using species comparisons and controlling for phylogeny, we investigated four hypotheses for the evolution of white undertail coverts in rails. We found little support for the hypothesis that white tails are sexually selected: white tails were not more common in species with polygamous as opposed to monogamous mating systems, species with sexual dimorphism, nor species that display their tails in courtship. Nor did our results support the hypothesis that white tail plumage evolved for intersexual competition during territorial interactions. Instead, we found that species that flock for at least part of the year and species found in open as opposed to concealing habitats were significantly more likely to have white undertail coverts. Rail species inhabiting concealing habitats are less commonly gregarious and more likely selected for crypsis. Using phylogenetically-controlled statistical inference we found that adaptation to open wetland habitats significantly precedes the evolution of white undertails, whereas gregariousness likely evolved later in some lineages. The inferred order of trait evolution suggests that this plumage characteristic could have been selected primarily for enhancement of an anti-predator signal rather than a social signal for conspecifics.

Genetic mapping of the female mimic morph locus in the ruff

BackgroundRuffs (Aves: Philomachus pugnax) possess a genetic polymorphism for male mating behaviour resulting in three permanent alternative male reproductive morphs: (i) territorial ‘Independents’, (ii) non-territorial ‘Satellites’, and (iii) female-mimicking ‘Faeders’. Development into independent or satellite morphs has previously been shown to be due to a single-locus, two-allele autosomal Mendelian mode of inheritance at the Satellite locus. Here, we use linkage analysis to map the chromosomal location of the Faeder locus, which controls development into the Faeder morph, and draw further conclusions about candidate genes, assuming shared synteny with other birds.ResultsSegregation data on the Faeder locus were obtained from captive-bred pedigrees comprising 64 multi-generation families (N = 381). There was no evidence that the Faeder locus was linked to the Satellite locus, but it was linked with microsatellite marker Ppu020. Comparative mapping of ruff microsatellite markers against the chicken (Gallus gallus) and zebra finch (Taeniopygia guttata) genomes places the Ppu020 and Faeder loci on a region of chromosome 11 that includes the Melanocortin-1 receptor (MC1R) gene, which regulates colour polymorphisms in numerous birds and other vertebrates. Melanin-based colouration varies with life-history strategies in ruffs and other species, thus the MC1R gene is a strong candidate to play a role in alternative male morph determination.ConclusionTwo unlinked loci appear to control behavioural development in ruffs. The Faeder locus is linked to Ppu020, which, assuming synteny, is located on avian chromosome 11. MC1R is a candidate gene involved in alternative male morph determination in ruffs.

Conspecific brood parasitism in the tropics: an experimental investigation of host responses in common moorhens and American purple gallinules

Species occupying a broad latitudinal range may show greater phenotypic plasticity in behavior than species with smaller ranges or more specific habitat requirements. This study investigates for the first time the occurrence of conspecific brood parasitism (CBP) in sympatric tropical populations of the common moorhen (Gallinula chloropus pauxilla Bangs) and the American purple gallinule (Porphyrula martinica L.). CBP occurred in at least 20% (N = 76) of common moorhen nests on the Rio Chagres in Panama. Half (N = 20) of the parasitic eggs were accepted, but 10 were destroyed or ejected from host nests. Introductions of experimental eggs into nests revealed hosts were more likely to accept parasitism later in the hosts laying period and during incubation, consistent with expectation of an adaptive response. CBP was not detected in a small sympatric population of American purple gallinules. Members of this population did not eject experimental eggs, suggesting a lack of experience with costly CBP. Contrasting ecological factors help explain why these two species of rail (Family Rallidae) differ in regard to CBP. Purple gallinule territories were sparse, owing to the distribution of preferred habitat. Moorhens flocked outside of the breeding season. They nested more synchronously, at higher densities, and primarily in ephemeral floating vegetation. Further, moorhens suffered a rate of nest loss nearly double that of American purple gallinules, and this increased over the course of the breeding season. Moorhen clutches were larger on average, and more variable in size than those of purple gallinules. Reproductive effort and rate (seasonality) constitute important life history differences between these species that may constrain the evolution of reproductive tactics. Comparing these sympatric populations, and others differing in life-history traits and ecological constraints, highlights the role of risk management in the evolution of CBP.

A genetic technique to identify the diet of cownose rays, Rhinoptera bonasus: analysis of shellfish prey items from North Carolina and Virginia

Cownose rays are implicated in the consumption of commercially important shellfish on the U.S. East Coast. We tested this assumption by developing a molecular technique for species identification from cownose ray gut contents. Digestive tracts sampled from 33 rays in Pamlico Sound, NC and Chesapeake Bay, VA contained pieces of partially-digested tissue, well-digested tissue, fluid, and minute shell fragments which made visual identification to the species level nearly impossible. We sequenced the cytochrome oxidase subunit I (COI) for seven locally acquired bivalve species, chosen for their commercial and ecological importance in NC and VA. Sequences were used to design species-specific primers for each bivalve species to amplify polymerase chain reaction (PCR) products. We designed primers such that PCR products were sufficiently different in size to be distinguishable from one another when resolved on an agarose gel, and multiplexing of several species in one reaction was possible. Digestive tract sample testing revealed that cownose rays in Chesapeake Bay ate stout tagelus and soft shell clams. There was no evidence of the rays in the study consuming commercially important oysters, hard clams, and bay scallops. Further sampling over an extended period of time and additional locations is required to confirm these results. Our diagnostic tests could easily be expanded to elucidate the impact of cownose ray predation on prey populations.

King Rails (Rallus elegans) Vary Building Effort and Nest Height in Relation to Water Level

Abstract. Breeding King Rails (Rallus elegans) have become more reliant on coastal marshes, but these are prone to variation in water level influenced by estuarine effluent and storm surge. Nest-building behavior in King Rails was studied in a natural coastal marsh subjected to a wind-driven tide system, where rapid water level rise from storm surge has led to nest inundation. To determine whether breeders exhibited plasticity in nest building in response to water level variation, nest height and water level were monitored at 2- to 3-day intervals, and video was used to quantify building behavior. Average height varied substantially among King Rail nests, indicating plasticity in overall building effort. King Rails constructed significantly taller nests at sites with greater variation in water level. Parents spent a greater proportion of time nest building when the water level was closer to the nest rim. The majority of nest accumulation occurred before laying ceased. Though King Rails continue to build through the nesting cycle, which is likely to counteract settling and improve the structural integrity of nests, they may not be able to increase nest height quickly enough to avoid flooding when faced with rapidly rising water.

Genetic analyses reveal cryptic introgression in secretive marsh bird populations

Abstract Hybridization is common in bird populations but can be challenging for management, especially if one of the two parent species is of greater conservation concern than the other. King rails (Rallus elegans) and clapper rails (R. crepitans) are two marsh bird species with similar morphologies, behaviors, and overlapping distributions. The two species are found along a salinity gradient with the king rail in freshwater marshes and the clapper in estuarine marshes. However, this separation is not absolute; they are occasionally sympatric, and there are reports of interbreeding. In Virginia, USA, both king and clapper rails are identified by the state as Species of Greater Conservation Need, although clappers are thought to be more abundant and king rails have a higher priority ranking. We used a mitochondrial DNA marker and 13 diagnostic nuclear single nucleotide polymorphisms (SNPs) to identify species, classify the degree of introgression, and explore the evolutionary history of introgression in two putative clapper rail focal populations along a salinity gradient in coastal Virginia. Genetic analyses revealed cryptic introgression with site‐specific rates of admixture. We identified a pattern of introgression where clapper rail alleles predominate in brackish marshes. These results suggest clapper rails may be displacing king rails in Virginia coastal waterways, most likely as a result of ecological selection. As introgression can result in various outcomes from outbreeding depression to local adaptation, continued monitoring of these populations would allow further exploration of hybrid fitness and inform conservation management.

Seasonal home range dynamics and sex differences in habitat use in a threatened, coastal marsh bird

Abstract A comprehensive understanding of spatiotemporal ecology is needed to develop conservation strategies for declining species. The king rail (Rallus elegans) is a secretive marsh bird whose range historically extended across the eastern United States. Inland migratory populations have been greatly reduced with most remaining populations inhabiting the coastal margins. Our objectives were to determine the migratory status of breeding king rails on the mid‐Atlantic coast and to characterize home range size, seasonal patterns of movement, and habitat use. Using radiotelemetry, we tracked individual king rails among seasons, and established that at least a segment of this breeding population is resident. Mean (±SE) home range size was 19.8 ± 5.0 ha (95% kernel density) or 2.5 ± 0.9 (50% kernel density). We detected seasonal variation and sex differences in home range size and habitat use. In the nonbreeding season, resident male home ranges coincided essentially with their breeding territories. Overwintering males were more likely than females to be found in natural emergent marsh with a greater area of open water. Females tended to have larger home ranges than males during the nonbreeding season. We report for the first time the use of wooded natural marsh by overwintering females. Brood‐rearing king rails led their young considerable distances away from their nests (average maximum distance: ~600 ± 200 m) and used both wooded natural and impounded marsh. King rails moved between natural marsh and managed impoundments during all life stages, but the proximity of these habitat types particularly benefitted brood‐rearing parents seeking foraging areas with shallower water in proximity to cover. Our results demonstrate the importance of interspersion of habitat types to support resident breeders. Summer draining of impounded wetlands that are seasonally flooded for wintering waterfowl allows regrowth of vegetation and provides additional habitat at a critical time for wading birds.