Sea surface temperature, rather than land mass or geographical distance, may drive genetic differentiation in a species complex of highly-dispersive seabirds

Abstract

Seabirds, particularly Procellariiformes, are highly mobile organisms with a great capacity for long dispersal, though simultaneously showing high philopatry, two conflicting characteristics that may lead to contrasted patterns of genetic population structure. Landmasses were suggested to explain differentiation patterns observed in seabirds, but philopatry, isolation-bydistance, segregation between breeding and non-breeding zones, and oceanographic conditions (sea surface temperatures) may also contribute to differentiation patterns. No study has simultaneously contrasted the multiple factors contributing to the diversification of seabird species, especially in the grey zone of speciation. We conducted a multi-locus phylogeographic study on a widespread shearwater species complex (Puffinus lherminieri/bailloni), showing highly homogeneous morphology. We sequenced three mitochondrial and six nuclear markers on all extant populations (five nominal lineages, 13 populations). We found sharp differentiation among populations separated by the African continent with both mitochondrial and nuclear markers, while only mitochondrial markers allowed characterizing the five nominal lineages. No differentiation could be detected within these five lineages, questioning the strong level of philopatry showed by these shearwaters. Finally, we propose that Atlantic populations likely originated from the Indian Ocean. Within the Atlantic, a stepping-stone process accounts for the current distribution. Based on our divergence times estimates, we suggest that the observed pattern of differentiation mostly resulted from variation in sea surface temperatures.

Translocation of mitochondrial DNA into the nuclear genome blurs phylogeographic and conservation genetic studies in seabirds

“…25% of discordant individuals for pax are also discordant for βfib , see electronic supplementary material, table S5b). Moreover, the patterns of discordance for numt sequences are similar to what we observed for nuclear markers [30] and could be explained by the same processes. We recently proposed that the aforementioned nuclear markers may reveal recent introgression and/or incomplete lineage sorting (ILS) in this species complex.…”

“…Digestion of linear DNA is an efficient way of removing numts when only orthologous mtDNA is desired [30] but has the drawback of requiring a substantial amount of DNA (starting with 1 µg of gDNA usually resulted in trace amounts of circular mtDNA post-exonuclease digestion). If mtDNA is fragmented, it will be digested as nuclear DNA.…”

“…Our dataset is an extension of a companion study [30], in which blood samples from a total of 228 individuals were obtained from Puffinus lheminieri and P . bailloni shearwaters, totalling 13 different breeding populations.…”

“…A portion of mt-cytb was amplified using shearwater-specific primers designed in [30] (forward: Cytb-F1-Puf-CRI, GGCCTACTACTAGCYATACA; reverse: Cytb-R4-PUF-CRI, GTTARGATGAATAGGTTRGCG), with the proof-reading Ex-Taq polymerase (Takara Bio Europe). The PCR amplification protocol is detailed in [30].

Figure 1Distribution of the breeding colonies sampled for this study.

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“…Our first aim consisted of evaluating the impact of these multiple copies on population-level statistics routinely used in genetic analyses, while our second aim consisted of evaluating to which extent numts affect the evolutionary scenarios obtained from mitochondrial sequences. We chose to target cytochrome-b ( mt-cytb ) because this mitochondrial gene is informative at the phylogeographic scale in this group of shearwaters [30] and has been a marker of choice for many seabird species (e.g. electronic supplementary material, table S1).…”