Independent evolution of intermediate bill widths in a seabird clade

Abstract

Interspecific introgression can occur between species that evolve rapidly within an adaptive radiation. Pachyptila petrels differ in bill size and are characterised by incomplete reproductive isolation, leading to interspecific gene flow. Salvin's prion (Pachyptila salvini), whose bill width is intermediate between broad-billed (P. vittata) and Antarctic (P. desolata) prions, evolved through homoploid hybrid speciation. MacGillivray's prion (P. macgillivrayi), known from a single population on St Paul (Indian Ocean), has a bill width intermediate between salvini and vittata and could also be the product of interspecies introgression or hybrid speciation. Recently, another prion population phenotypically similar to macgillivrayi was discovered on Gough (Atlantic Ocean), where it breeds 3 months later than vittata. The similarity in bill width between the medium-billed birds on Gough and macgillivrayi suggest that they could be closely related. In this study, we used genetic and morphological data to infer the phylogenetic position and evolutionary history of P. macgillivrayi and the Gough medium-billed prion relative other Pachyptila taxa, to determine whether species with medium bill widths evolved through common ancestry or convergence. We found that Gough medium-billed prions belong to the same evolutionary lineage as macgillivrayi, representing a new population of MacGillivray's prion that originated through a colonisation event from St Paul. We show that macgillivrayi's medium bill width evolved through divergence (genetic drift) and independently from that of salvini, which evolved through hybridisation (gene flow). This represents the independent convergence towards a similarly medium-billed phenotype. The newly discovered MacGillivray's prion population on Gough is of utmost conservation relevance, as the relict macgillivrayi population in the Indian Ocean is very small.

Keywords: Convergent evolution; Gough Island; MacGillivray’s prion; Pachyptila; Procellariidae; Procellariiformes.

Fig. 1

Locations of prions Pachyptila populations investigated around the Southern Ocean

Fig. 2

Differences in bill widths of adult larger-billed prions (Pachyptila). Box plot, Dunn’s homogenous subgroups (a–e), and sample sizes of the populations measured in this study. Box plots include medians, whiskers indicate variability outside the upper and lower quartiles (grey shaded block), and circles are outliers. Data from Masello et al. (2019) and references therein are shown here in green for comparison purposes; green triangles represent means for different colonies (turtur: 7; belcheri: 3; desolata: 7; salvini: 2; vittata: 1)

Fig. 3

Medium-joining haplotype network (A) and inferred Bayesian phylogeny (B) based on the combined sequence data for cyt b and COI for the prion taxa (Pachyptila) in this study. In the network, the circle size is proportional to haplotype frequency, hash marks crossing line connections represent mutational steps, and nodes without circles correspond to hypothetical haplotypes not sampled. In the inferred phylogeny, for clarity reasons, 95% HPD bars and probabilities are only shown for nodes with posterior probabilities > 0.5

Fig. 4

Genetic ancestry based on an 18 microsatellite loci data set for the prion taxa (Pachyptila) in this study. Genetic structure was modelled in STRUCTURE assuming admixture and the partitioning of genetic diversity into two (K = 2) and three (K = 3) populations (K4–10 shown in Supplemental Fig. S1). Each line on the plot represents an individual multilocus profile

Fig. 5

Ancestral state reconstruction of bill width at the root of the Pachyptila phylogeny. This posterior distribution of ancestral bill widths was inferred as a continuously varying trait using generalised least squares in BAYESTRAITS