David B. McDonald

Predicting fate from early connectivity in a social network

In the long-tailed manakin (Chiroxiphia linearis), a long-lived tropical bird, early connectivity within a social network predicts male success an average of 4.8 years later. Long-tailed manakins have an unusual lek mating system in which pairs of unrelated males, at the top of complex overlapping teams of as many as 15 males, cooperate for obligate dual-male song and dance courtship displays. For as long as 8 years before forming stable “alpha–beta” partnerships, males interact with many other males in complex, temporally dynamic social networks. “Information centrality” is a network connectivity metric that accounts for indirect as well as shortest (geodesic) paths among interactors. The odds that males would rise socially rose by a factor of five for each one-unit increase in their early information centrality. Connectivity of males destined to rise did not change over time but increased in males that failed to rise socially. The results suggest that network connectivity is important for young males (ages 1–6) but less so for older males of high status (ages 10–15) and that it is difficult to explain present success without reference to social history.

Evolutionary implications of divergent clines in an avian (Manacus: Aves) hybrid zone

Abstract A previous study of the hybrid zone in western Panama between white‐collared (Manacus candei) and golden‐collared manakins (M. vitellinus) documented the unidirectional introgression of vitellinus male secondary sexual traits across the zone. Here, we examine the hybrid zone in greater genetic and morphological detail. Statistical comparisons of clines are performed using maximum‐likelihood and nonparametric bootstrap methods. Our results demonstrate that an array of six molecular and two morphometric markers agree in cline position and width. Clines for male collar and belly color are similar in width to the first eight clines, but are shifted in position by at least five cline widths. The result is that birds in intervening populations are genetically and morphometrically very like parental candei, but males have the plumage color of parental vitellinus. Neither neutral diffusion nor nonlinearity of color scales appear to be viable explanations for the large cline shifts. Genetic dominance of vitellinus plumage traits is another potential explanation that will require breeding experiments to test. Sexual selection remains a plausible explanation for the observed introgression of vitellinus color traits in these highly dimorphic, polygynous, lek‐mating birds. Two other clines, including a nondiagnostic isozyme locus, are similar in position to the main cluster of clines, but are broader in width. Thus, introgression at some loci is greater than that detected with diagnostic markers. Assuming that narrow clines are maintained by selection, variation in cline width indicates that selection is not uniform throughout the genome and that diagnostic markers are under more intense selective pressure. The traditional focus on diagnostic markers in studies of hybrid zones may therefore lead to underestimates of average introgression. This effect may be more pronounced in organisms with low levels of genetic divergence between hybridizing taxa.

Correlates of male mating success in a lekking bird with male-male cooperation

Correlates of male mating success were examined in a population of long-tailed manakins, Chiroxiphia linearis, that included 270 colour-banded individuals. Long-tailed manakins have a lek mating system and male-male cooperation in courtship display. Multivariate analysis of behavioural variables indicated that female visitation correlated with the number of unison ‘toledo’ calls given by male partners. Given a female vist, copulatory success was correlated with the ‘butterfly’ display component of the dual-male dance. Both ‘toledo’ output and dance display differed significantly between perch-zones. Only six to eight partnerships in a local population of as many as 55 males per season performed call displays at a level (75–335 toledos per h) that was correlated with any female visitation. Data on crown plumage of female visitors suggested that younger females may have been less discriminating than were older females. The relationship between variance in mating success and the evolution of cooperative male display is discussed.

Cooperation Under Sexual Selection: Age-Graded Changes in a Lekking Bird

Long-tailed manakins, Chiroxiphia linearis, are birds with a lek mating system and male-male cooperation in courtship display. I studied male-male networks in a color-banded population in Monteverde, Costa Rica, from 1981 to 1987. Males displayed in scattered leks (75-300 m apart) comprising 3-15 males. Within each lek, an alpha and beta male, with strict relative dominance ranks, performed most of the courtship display. Of 50-60 active males per season, only 6-8 males were well-established alpha males in leks with consistent levels of dual-male displays (calls and dances). Demographic data suggest that males may be 8 yr of age or more before attaining beta status. Alpha tenure can last from two to at least four years. Alpha males were rarely or never seen in perch zones other than their primary perch zone (their area of dominance). Lower-ranking males maintained simultaneous affiliations with males in as many as six different zones. Each zone, therefore, acted as a hub in which males with different affiliations around the rim came into contact. Each of the six major perch zones shared at least one affiliate with each of the other zones, and roughly half the males in any particular zone were also known affiliates in one or more other zones. Marked changes occurred in male traits with increasing age and status: (1) significant declines in weight throughout the life span, without loss of dominance status; (2) a 4-yr delay in plumage maturation with distinct subdefinitive, transitional stages; (3) reduction in the number of perch zones with which older males maintained affiliations; and (4) increasing probability of copulatory success. The results are consistent with the hypothesis that subdefinitive plumages in this species serve primarily as accurate indicators of age, which in turn largely determines status, and that males queue for positions in an age-based dominance system. The results do not support the hypothesis that delayed plumage maturation involves mimicry or deceptive signaling by subdefinitive males (≤3 yr old) to high-ranking males (≥8 yr old). Of 85 males monitored from 1983 to 1986, copulations (N = 117) were distributed among 8 males. Four of these males accounted for over 90% of the copulations, with 67% accruing to one male. An index of the opportunity for sexual selection, to be used cautiously in interspecific comparisons, was estimated to range from 15.8 to 31.5 in four successive years. Direct benefits to cooperation by the beta male consisted of rare immediate copulations (N = 2) and eventual ascent to alpha status (N = 3). The high variance of mating success means few opportunities for success by younger males and should favor long-term strategies, such as cooperation and delayed plumage maturation, that enhance the prospects of future success.

SEXUAL SELECTION ON PLUMAGE AND BEHAVIOR IN AN AVIAN HYBRID ZONE: EXPERIMENTAL TESTS OF MALE-MALE INTERACTIONS

Abstract.— In western Panama, an unusual hybrid zone exists between white‐collared manakins, Manacus candei, and golden‐collared manakins, M. vitellinus. Unidirectional introgression of plumage traits from vitellinus into candei has created a region in which all definitively plumaged males have a collar that is lemon‐colored. These males are nearly indistinguishable from white‐collared candei genetically and morphometrically, but strongly resemble golden‐collared vitellinus due to the introgression of secondary sexual plumage traits, particularly the lemon‐colored collar. The introgression could be explained by sexual selection for golden‐collared traits or by a series of mechanisms that do not invoke sexual selection (e.g., neutral diffusion, dominant allele). Sexual selection on male‐male interactions implies behavioral differences among the plumage forms—specifically that golden‐ and lemon‐collared males should be more aggressive than white‐collared males. In contrast, the nonsexual hypotheses predict behavioral similarity between lemon‐ and white‐collared males, based on their nearly identical genetics. We tested the sexual selection hypothesis experimentally, by presenting males with taxidermic mounts of the three forms. As response variables, we monitored vocalizations and attacks on the mounts by replicate subject males. Both golden‐collared and lemon‐collared males were more likely to attack than were white‐collared males, as predicted under sexual selection but not by the nonsexual hypotheses. Lemon‐collared males were more vocally reactive than either parental form, contrary to the prediction of the nonsexual hypotheses. Our study demonstrates that sexual selection on male‐male interactions may play an important role in the dynamics of character evolution and hybrid zones.

Matrix Methods for Avian Demography

Demography is a tool for understanding population-level dynamics in terms of events (birth, death, maturation, etc.) at the level of the individual. Demographic models are a critical component of theory in population genetics, life history evolution, mating systems, and population biology. Demography is of fundamental concern to conservation biology; the demographic rather than genetic consequences of rarity may be the imminent threat to species facing rapid habitat destruction in many parts of the world (Lande, 1988b).

The genomic consequences of adaptive divergence and reproductive isolation between species of manakins

The processes of adaptation and speciation are expected to shape genomic variation within and between diverging species. Here we analyze genomic heterogeneity of genetic differentiation and introgression in a hybrid zone between two bird species (Manacus candei and M. vitellinus) using 59 100 SNPs, a whole genome assembly, and Bayesian models. Measures of genetic differentiation ( FST ) and introgression (genomic cline center [α] and rate [β]) were highly heterogeneous among loci. We identified thousands of loci with elevated parameter estimates, some of which are likely to be associated with variation in fitness in Manacus populations. To analyze the genomic organization of differentiation and introgression, we mapped SNPs onto a draft assembly of the M. vitellinus genome. Estimates of FST , α, and β were autocorrelated at very short physical distances (< 100 bp), but much less so beyond this. In addition, average statistical associations (linkage disequilibrium) between SNPs were generally low and were not higher in admixed populations than in populations of the parental species. Although they did not occur with a constant probability across the genome, loci with elevated FST , α, and β were not strongly co‐localized in the genome. Contrary to verbal models that predict clustering of loci involved in adaptation and isolation in discrete genomic regions, these results are consistent with the hypothesis that genetic regions involved in adaptive divergence and reproductive isolation are scattered throughout the genome. We also found that many loci were characterized by both exceptional genetic differentiation and introgression, consistent with the hypothesis that loci involved in isolation are also often characterized by a history of divergent selection. However, the concordance between isolation and differentiation was only partial, indicating a complex architecture and history of loci involved in isolation.

An introduced and a native vertebrate hybridize to form a genetic bridge to a second native species

The genetic impacts of hybridization between native and introduced species are of considerable conservation concern, while the possibility of reticulate evolution affects our basic understanding of how species arise and shapes how we use genetic data to understand evolutionary diversification. By using mitochondrial NADH dehydrogenase subunit 2 (ND2) sequences and 467 amplified fragment-length polymorphism nuclear DNA markers, we show that the introduced white sucker (Catostomus commersoni) has hybridized with two species native to the Colorado River Basin—the flannelmouth sucker (Catostomus latipinnis) and the bluehead sucker (Catostomus discobolus). Hybrids between the flannelmouth sucker and white sucker have facilitated introgression between the two native species, previously isolated by reproductive barriers, such that individuals exist with contributions from all three genomes. Most hybrids had the mitochondrial haplotype of the introduced white sucker, emphasizing its pivotal role in this three-way hybridization. Our findings highlight how introduced species can threaten the genetic integrity of not only one species but also multiple previously reproductively isolated species. Furthermore, this complex three-way reticulate (as opposed to strictly bifurcating) evolution suggests that seeking examples in other vertebrate systems might be productive. Although the present study involved an introduced species, similar patterns of hybridization could result from natural processes, including stream capture or geological formations (e.g., the Bering land bridge).

Actuarial Senescence and Demographic Heterogeneity in the Florida Scrub Jay

Analysis of mortality from a 25-yr sample of 380 Florida Scrub Jays, Aphel- ocoma c. coerulescens, shows that actuarial senescence (increase in mortality with age) occurs. This refutes the notion that adult mortality is independent of age in birds, and has important implications for evolutionary dynamics. We point to two major factors that may act to mask underlying patterns of actuarial senescence: (1) Selection through time (de- mographic heterogeneity): because selection inevitably weeds out lower quality individuals first, overall mortality may appear to be constant or even decreasing, despite an increasing force of mortality acting on birds of higher quality. (2) Conflicting processes: one source of mortality may act to decrease mortality over time (e.g., group size effects), while another acts to increase it (e.g., degenerative senescence). Age-specific data, measures of intrinsic quality that are independent of mortality, and exposure of sources of heterogeneity and of conflicting processes allow us to demonstrate a clear pattern of actuarial senescence in an unmanipulated, natural population of long-lived birds. The slow rate of increase in mortality is consistent with the hypothesis that mortality increases more slowly with age in birds than in mammals.

Genetic Structure of Cougar Populations Across the Wyoming Basin: Metapopulation or Megapopulation

Abstract We examined the genetic structure of 5 Wyoming cougar (Puma concolor) populations surrounding the Wyoming Basin, as well as a population from southwestern Colorado. When using 9 microsatellite DNA loci, observed heterozygosity was similar among populations (HO = 0.49–0.59) and intermediate to that of other large carnivores. Estimates of genetic structure (FST = 0.028, RST = 0.029) and number of migrants per generation (Nm) suggested high gene flow. Nm was lowest between distant populations and highest among adjacent populations. Examination of these data, plus Mantel test results of genetic versus geographic distance (P ≤ 0.01), suggested both isolation by distance and an effect of habitat matrix. Bayesian assignment to population based on individual genotypes showed that cougars in this region were best described as a single panmictic population. Total effective population size for cougars in this region ranged from 1,797 to 4,532 depending on mutation model and analytical method used. Based on measures of gene flow, extinction risk in the near future appears low. We found no support for the existence of metapopulation structure among cougars in this region.