The Genetics of Waterfowl Hybridization

Greylag ( anser) x Canada Goose (Branta canadensis)

Jente Ottenburghs Wageningen University Hasselt University (Belgium) – Bachelor Biology

Antwerp University (Belgium) – Master Biology: Evolution and Behavioral Biology

KHLim (Belgium) – Lector Chemistry

Wageningen University (the Netherlands) – PhD

De Volkskrant (the Netherlands) – Science Journalist

Karolinska Institutet (Sweden) – Postdoc

Uppsala University (Sweden) – Postdoc

Barnacle Goose (Branta leucopsis) How common is hybridization in ?

Suchetet (1896) Gray (1958) McCarthy (2006) No Hybridization 16% of species hybridize in the wild Natural Hybridization 22% when including captive hybrids Captive Hybridization

The Avian Hybrids Project http://avianhybrids.wordpress.com/

Ottenburghs et al. (2015) Ibis = Hybrid Heaven

Mute Swan (Cygnus olor) x (Anser anser) Mallard (Anas platyrhynchos) x Northern Pintail (A. acuta) “Swoose”

Wood Duck (Aix sponsa) x Chestnut Teal (Anas castanea) Anseriformes = Hybrid Heaven

Ottenburghs (2019) Avian Research Why do birds choose a partner from another species?

Barnacle Goose Greater White-fronted Goose

Lesser White-fronted Goose Ross’ Goose Hawaiian Goose Emperor Goose Ottenburghs et al. (2016) Frontiers in Zoology Argentine Ruddy Duck The consequences of hybridization: Introgression

https://biology.stackexchange.com/ Introgression is the exchange of genetic material

For example: humans and Neanderthals Adaptive Introgression: Exchanged DNA is beneficial

Anderson et al. (2009) Science Adaptive Introgression: Exchanged DNA is beneficial Darwin’s Finches American Buntings Genes involved in beak morphology Genes for adaptation to salty environment

Saltmarsh sparrow Nelson's sparrow

Lamichhaney et al. (2015) Nature Walsh et al. (2018) Evolution Hybrid Speciation: 1 + 1 = 3 House Sparrow x Spanish Sparrow = Italian Sparrow

Elgvin et al. (2017) Science Advances Hawaiian Duck

Mallard Laysan Duck Study System – The True Geese Livezey (1996) Donne-Gousse et al. (2002) Greater White-fronted Goose Gonzalez et al. (2009) (A. albifrons)

Lesser White-fronted Goose (A. erythropus)

Ruokonen et al. (2000) Lee et al. (2008)

Pink-footed Goose Taiga (A. brachyrhynchus) (A. fabalis) Phylogeny of geese not resolved Extensive Hybridization

What is the impact of hybridization on the evolutionary history of geese?

100bp PE 19 Goose Genomes 10-15X Coverage

Anser (“Grey Geese”) Anser (“White Geese”) Greater White-fronted Goose (A. albifrons) Snow Goose (A. caerulescens) Lesser White-fronted Goose (A. erythropus) Ross’ Goose (A. rossii) Pink-footed Goose (A. brachyrhynchus) Emperor Goose (A. canagicus) (A. serrirostris) (A. fabalis) Bar-headed Goose (A. indicus) Greylag Goose (A. anser) Swan Goose (A. cygnoides) Branta (“Black Geese”) Barnacle Goose (B. leucopsis) Canada Goose (B. canadensis) Cackling Goose (B. hutchinsii) Hawaii Goose (B. sandvicensis) Red-breasted Goose (B. ruficollis) Brent Goose (B. bernicla) [3 subspecies]

Estimating the Species Tree

Delsuc et al. 2005 Nature Reviews Genetics

Degnan & Rosenberg (2009) Trends in Ecology & Evolution Ottenburghs et al. (2016) Molecular Phylogenetics and Evolution

Finding Introgression D-statistic

ABBA BABA If D ≠ 0 and Z-score > 3 T=then there has been introgression

P1 P2 P3 O A B B A 18,937

B A B A 15,896

Outgroup

D = 0.087

Barnacle Cackling Canada Z-score = 4.32 Goose Goose Goose It’s not a tree but a network

Swan Goose Bar-headed Goose Greylag Goose

Taiga Bean Goose

Tundra Bean Goose Dark-bellied Brent Goose Pale-bellied Brent Goose Pink-footed Goose Black Brent Goose

Greater White-fronted Goose

Lesser White-fronted Goose

Red-breasted Goose

Snow Goose Ross’ Goose

Emperor Goose

Barnacle Goose

Cackling Goose Hawaiian Goose Canada Goose

Ottenburghs et al. (2017) BMC Evolutionary Biology Not only in birds... Hybridization Networks

Is the Red-breasted Goose a hybrid species?

Ottenburghs et al. (2017) BMC Evolutionary Biology Ottenburghs (2018) Ecology and Evolution What is a species?

The Biological Species Concept defines a species as members of populations that actually or potentially interbreed in nature What is a species? Mayden (1997): 24 species concepts • Agamospecies Concept (ASC) • Morphological Species Concept (MSC) • Biological Species Concept (BSC) • Non-dimensional Species Concept (NDSC) • Cladistic Species Concept (ClSC) • Phenetic Species Concept (PhSC) • Cohesion Species Concept (CSC) • Phylogenetic Species Concept (PSC) • Composite Species Concept (CpSC) • Diagnosable Version • Ecological Species Concept (EcSC) • Monophyly Version • Evolutionary Species Concept (ESC) • Diagnosable and Monophyly Version • Evolutionary Significant Unit (ESU) • Polythetic Species Concept (PtSC) • Genealogical Concordance Concept (GCC) • Recognition Species Concept (RSC) • Genetic Species Concept (GSC) • Reproductive Competition Concept (RCC) • Hennigian Species Concept (HSC) • Successional Species Concept (SSC) • Internodal Species Concept (ISC) • Taxonomic Species Concept (TSC) Speciation is a gradual process Species 1 Species 2 and different criteria arise at different times

Datasets Criteria Taxonomic grey zone

Morphological data Morphological species criteria

Social signals Species recognition criteria

Genomic data Phylogenetic species criteria

Ancestral population What is a species?

Taiga Bean Goose Tundra Bean Goose Subtle differences in beak morphology

Burgers et al. (1991) Ardea Different breeding sites and migration routes

Burgers et al. (1991) Ardea They can be separated genetically... Did Taiga and Tundra Bean Goose exchange DNA?

N0 N0

Ts Ts

NF NS NF NS

m mFS/mSF

N 0 N0 T s Ts

NF NS N N T F S m Tm

m /m FS SF mFS/mSF Taiga and Tundra Bean Goose separated about 2,5 million years ago, but they started hybridizing ca. 60,000 years ago.

N0

Ts

NF NS Tm

mFS/mSF Species 1 Species 2 Are they different species?

Criteria Taxonomic grey zone

Genetic differences

Morphological differences

Ecological differences

Taiga Bean Goose Tundra Bean Goose

Ancestral population