With the publication of ‘A History of Hybrids? Genomic Patterns of Introgression in the True Geese’ in BMC Evolutionary Biology, the three goose papers from my PhD thesis have made it into scientific journals. The trilogy is complete, but the story continues…
During my PhD, I studied the evolutionary history of the True Geese. This bird group contains about 17 species (depending on which authority you follow) and is traditionally divided into two genera: Anser and Branta. At the start of my PhD, I was surprised to find out that the phylogeny (i.e. evolutionary tree) of the geese was still unresolved. The failure to resolve the relationships between these bird species is probably due to high levels of hybridization. My goal was to solve this phylogenetic conundrum and further explore the influence of hybridization during the evolutionary history of the True Geese.
Part 1: Goose Hybrids
Although the main focus of my research was to quantify the effects of hybridization on an evolutionary timescale, I wanted to know the current state of events. How often do birders see hybrid geese? Which species are interbreeding? Are these hybrids fertile? And why does a goose choose a partner of another species? These questions formed the basis for part one of the goose trilogy. This first story was published in Frontiers in Zoology, entitled ‘Hybridization in Geese: A Review’.
It turns out that the majority of goose species have interbred at some point (in captivity or in the wild). Hybrids are thus common on a species-level, but rare on a per-individual level. The origin of particular goose hybrids is difficult to deduce but several mechanisms, such as interspecific nest parasitism and extra-pair copulations, are possible. The different mechanisms are not mutually exclusive and it is currently not possible to discriminate between these mechanisms without quantitative data.
Most hybrid geese are fertile; only in crosses between distantly related species do female hybrids become sterile. This fertility pattern, which is in line with Haldane’s Rule, may facilitate interspecific gene flow between closely related species. This finding is important for the other stories in the goose trilogy.
Part 2: A Tree of Geese
Before I could investigate the role of hybridization in goose evolution, I needed a proper phylogenetic framework. The construction of this framework was the focus of my second story, which was published in Molecular Phylogenetics and Evolution under the title ‘A Tree of Geese: A Phylogenomic Perspective on the Evolutionary History of True Geese‘.
For this study, I collected blood samples from all goose species. Sequencing the whole genome of these species provided me with a huge amount of data to resolve the phylogenetic tree of this bird group. I won’t bother you with the technical details (e.g., we opted for an exon-based approach with both concatenation and consensus analyses). Let’s jump straight to the main results!
The split between Anser and Branta was already well-established, but the relationships within these genera were contentious. Using whole genome data, I was able to resolve the phylogenetic relationships between the different goose species.
Within the genus Branta (commonly referred to as the Black Geese) there is a group of White-cheeked Geese – Canada Goose (B. canadensis), Cackling Goose (B. hutchinsii), Barnacle Goose (B. leucopsis) and Hawaiian Goose (B. sandvicensis) – and two basal splits – leading to Brent Goose (B. bernicla) and Red-breasted Goose (B. ruficollis).
In the genus Anser, the most basal split leads to the morphologically divergent Bar-headed Goose (A. indicus). Next, two main groups can be recognised: the White Geese – Snow Goose (A. caerulescens), Ross’ Goose (A. rossii) and Emperor Goose (A. canagicus) – and the Grey Geese – Greylag Goose (A. anser), Swan Goose (A. cygnoides), the White-fronted Geese (A. albifrons and A. erythropus) and the Bean Goose complex (A. fabalis, A. serrirostris and A. brachyrhynchus).
A molecular clock analysis indicated that the majority of speciation events took place at the end of the Pliocene. The approximate date of diversification coincides with the beginning of a period of climatic oscillations between 3.2 and 1.9 million years ago. This period was part of a fast global cooling trend, following the closure of the Panama Seaway and the uplifting of the Tibetan Plateau around four million years ago. This resulted in the formation of permanent Northern Hemisphere ice sheets, the establishment of a circumpolar tundra belt and the emergence of temperate grasslands, which opened up new ecological niches in which new groups of animals and plants were able to spread. The tundra habitat serves as breeding ground for geese, while the temperate grasslands act as wintering grounds where mate choice takes place. Moreover, these tundra and grassland habitats provided ample opportunity for geese to explore new ecological niches and diversify in beak morphology.
More importantly, the comparison of different gene trees revealed that different genes tell different stories. This observation, called gene tree discordance, can be caused by rapid speciation (leading to a phenomenon known as incomplete lineage sorting or ILS) and hybridization. Disentangling the contributions of ILS and hybridization is the focus of the third story.
Part 3: A History of Hybrids
And so we arrive at the final story in this trilogy where I explored the role of hybridization during the evolutionary history of the True Geese. As mentioned in the introduction, this story was published in BMC Evolutionary Biology, entitled ‘A History of Hybrids? Genomic Patterns of Introgression in the True Geese‘.
I found indications for ancient gene flow during the diversification of the True Geese and I was able to pinpoint several putative hybridization events. Specifically, in the genus Branta, both the ancestor of the White-cheeked Geese (Hawaiian Goose, Canada Goose, Cackling Goose and Barnacle Goose) and the ancestor of the Brent Goose hybridized with Red-breasted Goose.
The reconstruction of historical effective population sizes shows that most species experienced a steady increase during the Pliocene and Pleistocene (in agreement with the conclusions from story 2). These large effective population sizes might have facilitated contact between diverging goose species, resulting in the establishment of hybrid zones and consequent gene flow.
I can definitely conclude that the evolution of goose species follows a complex speciation model high levels of gene flow during species diversification. Unfortunately, I did not have the data to determine whether this gene flow is the outcome of (repeated) secondary contact or divergence-with-gene-flow. This warrants a population genomic approach whereby multiple individuals of one population are sequenced. In fact, this is exactly what I plan to do during my postdoc with Hans Ellegren at Uppsala University.
To be continued…
Ottenburghs, J., van Hooft, P., van Wieren, S.E., Ydenberg, R.C. & Prins, H.H.T. (2016). Hybridization in Geese: A Review. Frontiers in Zoology. 13:20 DOI: 10.1186/s12983-016-0153-1
Ottenburghs, J., Megens, H.-J., Kraus, R.H.S., Madsen, O., van Hooft, P., van Wieren, S.E., Crooijmans, R.P.M.A., Ydenberg, R.C., Groenen, M.A.M. & Prins, H.H.T. (2016). A Tree of Geese: A Phylogenomic Perspective on the Evolutionary History of True Geese. Molecular Phylogenetics and Evolution. 101:303-313 doi:10.1016/j.ympev.2016.05.021
Ottenburghs, J., Megens, H.-J., Kraus, R.H.S., van Hooft, P., van Wieren, S.E., Crooijmans, R.P.M.A., Ydenberg, R.C., Groenen, M.A.M. & Prins, H.H.T. (2017). A History of Hybrids? Genomic Patterns of Introgression in the True Geese. BMC Evolutionary Biology. 17:201 https://doi.org/10.1186/s12862-017-1048-2