Arctic Sharks: A Story of Ice-olation and Hybridization

Genetic study finds hybridization between Greenland Sharks and Pacific Sleeper Sharks. The researchers propose a model of ‘ice-olation with migration’.

Although this blog is about hybridization in birds, I will occasionally write about other taxonomic groups. This week, I came across a genetic shark study by Ryan Walter (California State University) and colleagues in the journal Ecology and Evolution. For several reasons (see further down), I could not resist fabricating a blog post on this shark story.

 

A Shark Tale

The Simniosidae is a family of sharks known as ‘sleeper sharks because of their apparent slow swimming. The recent study focuses on two species: the Greenland Shark (Somniosus microcephalus) and the Pacific Sleeper Shark (S. pacificus). The Greenland Shark ranges from the Canadian Arctic to the south of Norway, while the Pacific Sleeper Shark occurs from the Bering Street throughout the Pacific (hence the name) into the Southern Ocean. Previous studies, based on mitochondrial DNA (mtDNA) showed that both species can be distinguished from one another despite their physical resemblance.

 

greenland shark

A Greenland Shark (Simniosus microcephalus)

 

The researchers collected samples of 247 sharks across their extensive distribution. They sequences mtDNA and several nuclear markers. The genetic data confirmed previous studies; the species could be easily kept apart. However, some individuals were a genetic mixture of both species, suggesting hybridization. Further analyses (Isolation-with-Migration models for the curious readers) confirmed this suggestion. It turned out that genes have been flowing from Pacific Sleepers Sharks into Greenland Shark populations.

To explain this findings, the authors introduce a model of ‘ice-olation with migration’. Apart from being a great play of words, this model nicely places the genetic data in a climatic context. About 2.5 million years ago, a drastic reduction in global temperatures occurred. This decline resulted in sea ice formation in polar regions. The spreading of thick sea ice in combination with the submerged mountains of the Arctic probably reduced the connectivity between different shark populations. During this isolation, the shark populations diverged genetically. In periods when the climate warmed and the ice melted, the sharks re-established contact and hybridized.

 

seal broken

Another wordplay…

 

Why this blog post?

This cool story caught my eye for several reasons:

  1. Sharks! Who doesn’t like sharks? Okay, they are not birds, but they are sharks!
  2. After my PhD, I briefly worked for the science department at a Dutch newspaper (De Volkskrant). One of my most successful stories was about the Greenland Shark which can live up to 400 years! Here is the link (in Dutch).
  3. The climatic conditions that influenced the evolutionary history of these sharks is very similar to the conditions that drove the evolution of geese. Here is a quote from one of my papers on geese: “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.” Do you notice the resemblance.
  4. And of course, the great wordplay in the title (Ice-olation). Priceless!

 

References

Walter, R. P., D. Roy, N. E. Hussey, B. Stelbrink, K. M. Kovacs, C. Lydersen, B. C. McMeans, J. Svavarsson, S. T. Kessel and S. Biton Porsmoguer (2017). Origins of the Greenland shark (Somniosus microcephalus): Impacts of ice‐olation and introgression. Ecology and Evolution.

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Hybrid Owls: Californian Contacts and Mediterranean Migrants

Who doesn’t like owls? Silently gliding through the night, with their big eyes and flexible neck. And they even hybridize!

A wise old owl sat on an oak;
The more he saw the less he spoke;
The less he spoke the more he heard;
Why aren’t we like that wise old bird?

– Old Nursery Rhyme

 

When you look up the definition for hybridization in the English Oxford Dictionary, it states that hybridization is “The process of an animal or plant breeding with an individual of another species or variety.” Most people think that hybrids are the outcome of different species interbreeding (such as a lion and a tiger), but the definition also mentions variety. Indeed, hybrids between varieties, often referred to as subspecies, are also possible. Two recent studies on owls emphasize this possibility. Mark Miller (U.S. Geological Survey) and colleagues investigated a hybrid zone between subspecies of Spotted Owl (Strix occidentalis) in northern California. In Europe, Reto Burri (Uppsala University), Sylvain Antoniazza (University of Lausanne) and others focused on color morphs of the Barn Owl (Tyto alba).

 

A hybrid zone without hybrids

The study of hybridization between Northern Spotted Owls (S. o. caurina) and California Spotted Owls (S. o. occidentalis) has a long history (see the Strigiformes page for an overview of the publications). Among others, George F. Barrowclough and Susan M. Haig have unraveled the interactions between these subspecies. This new study provides a detailed genetic perspective on the hybrid zone in Northern California. In the contact zone, more than half of the individuals showed evidence of hybrid ancestry. The distribution of admixed owls suggests that the hybrid zone is moving north.

Surprisingly, no first generation (F1) hybrids were detected. Perhaps some hybrid owls were wrongly classified in the analyses or maybe the researchers did not sample F1-hybrids. It could also be that there is no recent hybridization. Several changes in the Californian landscape might have reduced the connectivity between different owl populations. In particular, the authors point to the Fountain Fire of 1992 which occurred at the intersection of the subspecies’ habitat.

 

SpottedOwl.jpg

A Northern Spotted Owl

 

Around the Mediterranean

Barn Owls gradually changes from white in Iberia to dark rufous in Northeastern Europe. In this study, researchers show that the rufous coloration is linked to a recent variant of the MC1R gene. More interestingly (from a hybridization point of view), Barn Owls seemed to have colonized western Europe in a ring around the Mediterranean. At a secondary contact zone in Greece there is evidence for limited genetic exchange. This pattern is reminiscent of ring species, i.e. populations with a ring-like distribution around a geographic barrier that are interconnected by gene flow. In recent years, it became obvious that most classical ring species do not adhere to this strict definition. Can the Barn Owl pass the test?

BarnOwls

The putative expansion routes and Greek second contact zone of the Barn Owl (adapted from Burri et al. 2016)

 

 

References

Burri, R., S. Antoniazza, A. Gaigher, A. L. Ducrest, C. Simon, L. Fumagalli, J. Goudet and A. Roulin (2016). The genetic basis of color‐related local adaptation in a ring‐like colonization around the Mediterranean. Evolution 70(1): 140-153.

Miller, M. P., T. D. Mullins, E. D. Forsman and S. M. Haig (2017). Genetic differentiation and inferred dynamics of a hybrid zone between Northern Spotted Owls (Strix occidentalis caurina) and California Spotted Owls (S. o. occidentalis) in northern California. Ecology and Evolution.

 

These papers have been added to the Strigiformes page.

The Beak of the Bullfinch: Remains of an Extinct Bird Species Found on the Azores

There used to be more than one Azores Bullfinch.

The Azores Bullfinch (Pyrrhula murina) is one of the rarest songbirds on this planet. And I have seen it! In 2011, I travelled to the Azores, a Portugese archipelago in the middle of the Atlantic Ocean, to collect snails for my Master thesis. But I was on a secret mission, I wanted to see the Azores Bullfinch, also known as Priolo. This small passerine only occurs on the island of Sao Miguel, where it is restricted to a small patch of native laurasilva forest. In 2008, the population was estimated at about 800 individuals. During one of the expeditions into the forest, I noticed a bird hopping around in the bushes. It turned out to be a Priolo! Here is one of the pictures I was able to make.

 

12-05_2011_Priolo1

 

A recent study, published in the scientific journal Zootaxa, reveals that there used to be another species of finch on the Azores. Researchers found bones in a small cave on the island of Graciosa. The bones showed that the extinct species – named Pyrrhula crassa – was larger than its living relatives. The evolutionary history of this second Azores bullfinch remains a mystery. Who knows how many other bullfinches inhabited the Azores in the past?

 

finches

From top to bottom: the Eurasian Bullfinch (P. pyrrhula), Azores Bullfinch (P. murina) and the extinct P. crassa. The colors of the newly described species are speculative (adapted from Rando et al. 2017).

 

References

Rando, J., Pieper, H., Olson, S. L., Pereira, F. & Alcover, J. 2017. A new extinct species of large bullfinch (Aves: Fringillidae: Pyrrhula) from Graciosa Island (Azores, North Atlantic Ocean). Zootaxa, 4282: 567-583.

Two Crow Hybrid Zones for the Price of One!

The comparison of two Crow hybrid zones reveals that history does not always repeats itself. Genomically, that is.

How species originate and adapt to new environments are some of the central questions in evolutionary biology. With the advent of genomic data, it has become possible to unravel the genomic basis of speciation and adaptation. And hybrid zones can serve as the ideal laboratories for testing new ideas.

One of the most widely studied hybrid zones concerns the contact zone between Hooded Crow (Corvus cornix) and Carion Crow (C. corone) in Europe (you can read more about it here).  A recent study revealed that several genomic regions were not exchanged between these hybridizing species (Poelstra et al. 2014). One of these regions harbored genes related to pigmentation and visual perception. Given that Hooded Crow and Carrion Crow differ in their color patterns, this genomic region could be crucial in the (probably still ongoing) speciation process.

 

Ottenburghs-Crows

Hooded Crow (front) and Carrion Crow

 

Thus, the European crow hybrid zone provided important insights into the genomic basis of speciation. But it gets ever better! Did you know that there is another crow hybrid zone in Siberia? In eastern Russia, Hooded Crow is hybridizing with the all-black Eastern Carrion Crow (C. orientalis). An almost perfect replicate of the hybrid zone in Europe!

 

Eastern Carrion Crow.jpg

An Eastern Carrion Crow

 

This set-up, two hybrids zones between species at different stages of speciation, provides an excellent opportunity to check whether the same genomic regions are involved. So, Nagarjun Vijay (Uppsala University) and colleagues sequenced and compared 124 genomes of different crow populations. They found that different genomic regions are under selection in the different hybrid zones. In the figure below, you can see the genomic comparison between Hooded Crow and Carrion Crow (above) and between Hooded Crow and Eastern Carrion Crow (below). Pay attention to the red dots, which represent genomic regions that are different between the species. If you move across the genomes, you will see that (with some exceptions) different genomic regions stand out in the two hybrid zones. Clearly, speciation does not repeat itself here.

Crow Genomes

The genomic landscape of crows (adapted from Vijay et al. 2016)

 

References

Poelstra, J. W., Vijay, N., Bossu, C. M., Lantz, H., Ryll, B., Muller, I., Baglione, V., Unneberg, P., Wikelski, M., Grabherr, M. G. & Wolf, J. B. W. (2014). The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344, 1410-1414.

Vijay, N., C. M. Bossu, J. W. Poelstra, M. H. Weissensteiner, A. Suh, A. P. Kryukov and J. B. Wolf (2016). Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex. Nature communications 7: 13195.

 

This paper has been added to the Corvidae page

A Northern and a Southern Perspective on Hybrids between Golden-winged and Blue-winged Warbler

Two recent studies provide insights into the genetics and migration of  two hybridizing Vermivora species. One study turns its attention to the north, whereas the other study focuses on the south.

Over the last 150 years, humans have converted large forest areas into agricultural fields in eastern North America. These habitat changes have facilitated contact between some geographically isolated bird species, often resulting in hybridization.

One example of such secondary contact is the story of Golden-winged (Vermivora chrysoptera) and Blue-winged Warblers (V. pinus). These two species were separated by large patches of forest. The conversion of this forest to agriculture enabled the Blue-Winged Warbler to spread north where it occasionally hybridized the Golden-winged Warbler. The combination of habitat loss and hybridization resulted in the decline of the latter species. The Golden-winged Warbler is now one of the most rapidly declining bird species in North America. Recently, two new studies have been added to the growing literature on the interactions of these small passerines (see here for an overview). One study looks at the final frontier in the north, while the other study focuses on migration to the south.

 

To The North

Previous studies documented extensive exchange of genetic material between these warblers (a process known as introgression). One exception was Manitoba in Canada. Laurel Moulton (University of Manitoba, Canada) and colleagues reassessed the genetic status of the Golden-winged Warbler in this area. Sampling over 200 birds between 2011 and 2014, they found 10 hybrids. It turns out that there is some genetic introgression in Manitoba, but the levels of introgression are the lowest across the range of Golden-winged Warbler. Hence, Manitoba can be seen as an important refuge for Golden-winged Warbler, where it is safe from the expanding Blue-winged Warbler. For now…

 

Golden-winged Warbler

A Golden-winged Warbler (from allaboutbirds.com)

 

To The South

Another recent study focused on a mixed population in the Jefferson and Lewis counties of New York. Ruth Bennett (Cornell University, Ithaca, NY) and colleagues attached geo-locators to 10 Golden-winged Warblers, 10 Blue-winged Warblers and 5 hybrids in order to investigate their migratory strategies. Given the genetic similarity between these species, the researchers expected to uncover similar migration routes.

The next year, data from 7 of the 25 birds were recovered. Two Golden-winged Warblers spend their winter in northern Colombia, while three Blue-winged Warblers flew to the Yucatan peninsula in Mexico and the western tip of Cuba. Two hybrids showed an intermediate choice and wintered in Cuba and Nicaragua. These results confirm the notion that migratory behavior is heritable in passerines with genetic hybrids showing intermediate strategies (see here).

 

Migration warblers

Wintering areas for Blue-winged Warbler (diamonds), Golden-winged Warbler (circles) and their hybrids (squares). Adapted from Bennett et al. (2017).

 

References

Bennett, Ruth E, Sara Barker Swarthout, Jeffrey S Bolsinger, Amanda Rodewald, Kenneth V Rosenberg, and Ron Rohrbaugh. 2017. ‘Extreme genetic similarity does not predict non‐breeding distribution of two closely related warblers’, Journal of Field Ornithology.

Moulton, Laurel L, Rachel Vallender, Christian Artuso, and Nicola Koper. 2017. ‘The final frontier: early-stage genetic introgression and hybrid habitat use in the northwestern extent of the Golden-winged Warbler breeding range’, Conservation Genetics: 1-7.

 

The papers have been added to the already quite extensive Parulidae page.