Frode Jacobsen

Extrapair mating between relatives in the barn swallow: a role for kin selection?

Why do females of many species mate with more than one male? One of the main hypotheses suggests that female promiscuity is an insurance mechanism against the potential detrimental effects of inbreeding. Accordingly, females should preferably mate with less related males in multiple or extrapair mating. Here we analyse paternity, relatedness among mating partners, and relatedness between parents and offspring, in the socially monogamous North American barn swallow (Hirundo rustica erythrogaster). In contrast to the inbreeding avoidance hypothesis, we found that extrapair mating partners were more related than expected by random choice, and tended to be more related than social partners. Furthermore, extrapair mating resulted in genetic parents being more related to their extrapair young than to their withinpair young. We propose a new hypothesis for extrapair mating based on kin selection theory as a possible explanation to these findings.

Male tail streamer length predicts fertilization success in the North American barn swallow (Hirundo rustica erythrogaster)

In socially monogamous species, extra-pair paternity has the potential to increase the variance in male reproductive success, thereby affecting the opportunity for sexual selection on male extravagant ornamentation. In the European barn swallow (Hirundo rustica rustica), the tail streamer length is a sexually selected male ornament and an honest indicator of viability. The North American barn swallow (Hirundo rustica erythrogaster) also shows sexual dimorphism in tail streamer length, but whether this trait holds the same signalling function in this subspecies is a controversial issue, and the available literature is presently scarce. Here, we present data on paternity in the North American barn swallow, including a complete sampling of extra-pair sires in four colonies. We analysed how extra-pair paternity affected the variance in male fertilization success and examined whether male tail streamer (i.e. the outermost tail feather) length correlated with fertilization success (n=86 males). Extra-pair paternity constituted 31% of all offspring and significantly increased the variance in male fertilization success. The number of offspring sired by extra-pair males accounted for almost half of the total variance in male fertilization success. Males with naturally long tail streamers had a higher fertilization success than males with shorter tail streamers, and this pattern was mainly caused by a higher extra-pair success for males with long tail streamers. Males with long tail streamers also paired with early breeding females in prime body condition. These results are consistent with the idea that there is directional sexual selection on male tail streamer length, possibly mediated through male extra-pair mating success or the timing of breeding onset.

Age before beauty? Relationships between fertilization success and age-dependent ornaments in barn swallows

When males become more ornamented and reproduce more successfully as they grow older, phenotypic correlations between ornament exaggeration and reproductive success can be confounded with age effects in cross-sectional studies, and thus say relatively little about sexual selection on these traits. This is exemplified here in a correlative study of male fertilization success in a large colony of American barn swallows (Hirundo rustica erythrogaster). Previous studies of this species have indicated that two sexually dimorphic traits, tail length and ventral plumage coloration, are positively correlated with male fertilization success, and a mechanism of sexual selection by female choice has been invoked. However, these studies did not control for potential age-related variation in trait expression. Here, we show that male fertilization success was positively correlated with male tail length but not with plumage coloration. We also show that 1-year-old males had shorter tails and lower fertilization success than older males. This age effect accounted for much of the covariance between tail length and fertilization success. Still, there was a positive relationship between tail length and fertilization success among older males. But as this group consisted of males from different age classes, an age effect may be hidden in this relationship as well. Our data also revealed a longitudinal increase in both tail length and fertilization success for individual males. We argue that age-dependent ornament expression and reproductive performance in males complicate inferences about female preferences and sexual selection.

Species tree inference in a recent radiation of orioles (Genus Icterus): Multiple markers and methods reveal cytonuclear discordance in the northern oriole group

Recent computational advances provide novel opportunities to infer species trees based on multiple independent loci. Thus, single gene trees no longer need suffice as proxies for species phylogenies. Several methods have been developed to deal with the challenges posed by incomplete and stochastic lineage sorting. In this study, we employed four Bayesian methods to infer the phylogeny of a clade of 11 recently diverged oriole species within the genus Icterus. We obtained well-resolved and mostly congruent phylogenies using a set of seven unlinked nuclear intron loci and sampling multiple individuals per species. Most notably, Bayesian concordance analysis generally agreed well with concatenation; the two methods agreed fully on eight of nine nodes. The coalescent-based method ∗BEAST further supported six of these eight nodes. The fourth method used, BEST, failed to converge despite exhaustive efforts to optimize the tree search. Overall, the results obtained by new species tree methods and concatenation generally corroborate our findings from previous analyses and data sets. However, we found striking disagreement between mitochondrial and nuclear DNA involving relationships within the northern oriole group. Our results highlight the danger of reliance on mtDNA alone for phylogenetic inference. We demonstrate that in spite of low variability and incomplete lineage sorting, multiple nuclear loci can produce largely congruent phylogenies based on multiple species tree methods, even for very closely-related species.

Colonization of South America from Caribbean Islands Confirmed by Molecular Phylogeny with Increased Taxon Sampling

Abstract. A previous phylogeny of New World orioles (Icterus) suggested a possible example of island-to-mainland colonization. Using two mitochondrial genes (cytochrome b and ND2), that study showed that 43 of the recognized species/ subspecies are divided into three clades (A, B, C). Because of a lack of fresh tissue, however, two key taxa—the South American Orange-crowned Oriole (I. auricapillus) and the Caribbean Hispaniola Oriole (I. dominicensis dominicensis)—were missing from that analysis. To complete the phylogeny, we sequenced both genes for these taxa and reconstructed a well-supported phylogeny via parsimony and maximum-likelihood analyses. The addition of I. d. dominicensis to the phylogeny confirms that the Greater Antillean Oriole (I. dominicensis) is polyphyletic, and taxonomic revision of this species complex is warranted. Also, the placement of I. auricapillus and I. d. dominicensis within clade A has important implications for biogeography. The revised phylogeny implies that clade A orioles colonized mainland South America from Caribbean islands. Orioles thus provide a striking example of reverse colonization that contradicts the traditional assumption in island biogeography of mainland-to-island colonization.

No evidence of paternal genetic contribution to nestling cell-mediated immunity in the North American barn swallow

Females involved in extrapair mating are generally thought to obtain indirect benefits through increased offspring quality. We investigated this in the barn swallow, Hirundo rustica , a socially monogamous passerine in which females seem to have a preference for elaborately ornamented, high-quality males, both as social and extrapair mating partners. In this species, a variety of parasites and pathogens can potentially infect individuals, both during the nestling stage and later in life. The ability to cope with infections and hence the quality of the immune system may therefore have immediate survival or future fitness consequences. To evaluate whether females engage in extrapair mating to increase offspring cell-mediated immunity, a pivotal component of the avian immune system, we experimentally challenged nestling immunity. Body condition, rearing environment and gender affected the ability of nestlings to mount an immune response. Contrary to a prediction derived from the ‘genetic quality’ hypothesis, our results revealed no enhanced cell-mediated immune responsiveness in extrapair young compared to their maternal half-siblings reared in the same brood. Female barn swallows therefore do not seem to mate with multiple males in order to increase nestling cell-mediated immunity. Although we cannot reject the possibility that extrapair mating is beneficial to female barn swallows, our results offer no support to the hypothesis that females obtain genetic benefits through extrapair fertilizations.

Coalescent analyses show isolation without migration in two closely related tropical orioles: the case of Icterus graduacauda and Icterus chrysater.

The Isthmus of Tehuantepec has played an important role in shaping the avian diversity of Mexico, as well as the rest of the Western Hemisphere. It has been both a barrier and a land connector between North and South America for many groups of birds. Furthermore, climatic change over the Pleistocene has resulted in ecological fluctuations that led to periods of connection and isolation of the highlands in this area. Here we studied the divergence of two species of orioles whose distribution in the highlands is separated by the lowlands of the Isthmus of Tehuantepec: Icterus graduacauda (west of the Isthmus) and Icterus chrysater (east of the Isthmus). We sequenced multiple loci (one mitochondrial gene and six nuclear introns) and performed coalescent analyses (Isolation with Migration) to test whether their divergence resulted from prior occupancy of the ancestral area followed by a vicariant event or recent dispersal from one side or the other of this Isthmus. Results strongly indicate a vicariant event roughly 300,000 years ago in the Pleistocene followed by little or no gene flow. Both mitochondrial and nuclear genes show that the Isthmus of Tehuantepec is a strong barrier to gene flow. Thus, these two species appear to not exchange genes despite their recent divergence and the close geographic proximity of their ranges.

Extensive introgressive hybridization within the northern oriole group (Genus Icterus) revealed by three-species isolation with migration analysis

Until recently, studies of divergence and gene flow among closely-related taxa were generally limited to pairs of sister taxa. However, organisms frequently exchange genes with other non-sister taxa. The “northern oriole” group within genus Icterus exemplifies this problem. This group involves the extensively studied hybrid zone between Baltimore oriole (Icterus galbula) and Bullocks oriole (I. bullockii), an alleged hybrid zone between I. bullockii and black-backed oriole (I. abeillei), and likely mtDNA introgression between I. galbula and I. abeillei. Here, we examine the divergence population genetics of the entire northern oriole group using a multipopulation Isolation-with-Migration (IM) model. In accordance with Haldanes rule, nuclear loci introgress extensively beyond the I. galbula–I. bullockii hybrid zone, while mtDNA does not. We found no evidence of introgression between I. bullockii and I. abeillei or between I. galbula and I. abeillei when all three species were analyzed together in a three-population model. However, traditional pairwise analysis suggested some nuclear introgression from I. abeillei into I. galbula, probably reflecting genetic contributions from I. bullockii unaccounted for in a two-population model. Thus, only by including all members of this group in the analysis was it possible to rigorously estimate the level of gene flow among these three closely related species.

Increasing evidence of the role of gene flow in animal evolution: hybrid speciation in the yellow-rumped warbler complex

In this issue of Molecular Ecology, Brelsford et al. (2011) present strong evidence for a case of hybrid speciation within the yellow‐rumped warbler complex. Although homoploid hybrid speciation has now been documented in many animals ( Mallet 2007 ), it seems rare in tetrapods ( Mavárez & Linares 2008 ) and it has barely even been mentioned in birds ( Price 2008 ). Brelsford and colleagues thus present the first detailed molecular evidence suggesting that hybrid speciation can occur in birds. Brelsford et al. (2011) posit that Audubon’s warbler (Dendroica auduboni) constitutes a hybrid species originating from the admixture of two distinct parental lineages, represented today by myrtle warbler (D. coronata) and black‐fronted warbler (D. nigrifrons). The authors present three major lines of molecular evidence suggesting that this is not simply a case of a hybrid swarm or limited introgression.