Managing wild-domestic hybridization:
How can genomics help?
Widespread “releases” of captive individuals
What is genomics?
Genomic extinction of westslope cutthroat trout
Why are hybrids so successful?
-----------------Identifying genomic regions under selection in
hybrid swarms
hybrida: the Latin
word for a piglet
resulting from the
union of a wild boar
and a tame sow.
Derived from the
Greek hubris, meaning
“arrogance or insolence
against the gods”.
Occurrence of large-scale releases
Genetic effects of releases
Hybridization
Another concern is that the domestic elk, which could be
unafraid of humans and overly docile, will breed with wild
elk and dilute the native gene pool.
“Local elk should be displaying superior genetics,” he said.
“Elk from other places may not be as well-adapted.”
But, Lawrence, Chief of Animal Health and Livestock for
the Idaho Agriculture Department, said the so-called
dumbing-down of the gene pool is an overblown worry.
"They're the same species," she said. "The traits for
surviving in the wild are the same. An elk will not come
out different colors if they breed."
The captive population of the European wildcat is a hybrid
swarm with mostly domestic cat nuclear and mtDNA.
2010
What is “Genomics”?
Broad Sense: The use of many (thousands) of
markers throughout the genome.
Narrow Sense: The use of tens of thousands of
markers located on an assembled
genome.
blue - traditional
red – “genomics”
The genomic effects of
inbreeding
2 discrete IBD
chromosome
segments
IBD = identical by descent
F = ∑ all ROH
lengths/genome size = F (the
true proportion of the
What is possible with whole genome
sequence and a good genome
assembly?
~20 Mb IBD segment
Chromosomal position (Mb)
Shorter IBD segments (usually
caused by more distant common
ancestors)
F can be measured with incredible accuracy/precision
using whole genome sequences when there is a good
assembly!
“Hybrid” tracts
May 2010
An estimated 3% of the
human genome of Europeans
resulted from hybridization
between modern humans and
Neandertals some 50,000
years ago
2001. Trends in
Ecology & Evolution
16:613-622.
Westslope cutthroat trout
(WCT)
Oncorhynchus clarkii lewisi
Yellowstone cutthroat trout
(YCT)
O. c. bouvieri
Rainbow trout
(RT)
O. mykiss
(Illustrations by Joseph R. Tomelleri)
A history of markers to study hybridization between
westslope cutthroat and rainbow trout:
1975
1980
1990
2000
2010
2014
Allozymes
mtDNA
PCR of interspersed nuclear elements
Microsatellites
In/Dels
SNPs
RADs (>3,000 diagnostic SNPs)
“Total” genome assembly
Hybrid swarm in Forest Lake, Montana
Hybrid swarm of native westslope (WCT) and
introduced Yellowstone cutthroat trout (YCT).
W= homozygous WCT; WY=heterozygous; Y= homozygous YCT
Hybrid swarm: all individuals are hybrids by varying
numbers of generations of backcrossing with parental types
and mating among hybrids.
mtDNA
p = proportion of WCT admixture
Conclusions
(1) All 8 nuclear loci show similar amounts of
admixture.
No evidence for differential rates of
introgression because of natural selection.
(2) Frequency of mtDNA genotype of native fish
generally greater than nuclear alleles.
Native females appear to have greater relative
fitness than native males.
<1%
admixture
WCT
1,333 sample sites
>20,000 individuals
Photo by Judy Smith Rushing
Examined hybridization in 42 putative
WCT samples from Flathead River.
Hybridization
widespread
(1985)
North Fork
WCT (n=17)
Hybridized (n=25)
Middle Fork
Flathead Lake
Hybridization
spreading
(2000)
North Fork
WCT (n=17)
Hybridized (n=17)
Hybridized post-1985
(n=8)
Middle Fork
Flathead Lake
Westslope cutthroat trout (WCT) and the
US Endangered Species Act (ESA)
• Formal petition in 1997 to list.
• USFWS (1999) found not warranted because of widespread
distribution and current status of the overall WCT population.
• Lawsuit argued that this finding was incorrect because it included
hybridized populations as WCT.
• Court (2002) ruled that this finding was not based on best available
science and ordered USFWS to reconsider whether to list
WCT after taking into account prevalence of hybridization.
Alternative 1: Include only non-hybridized WCT.
Alternative 2: Include WCT populations with less than 10%
admixture.
Alternative 3: Include all populations that have the
morphological attributes of WCT.
Our Recommendation: WCT are WCT.
Alternative 1: Only non-hybridized (<1%
admixture) populations should be included as
WCT in the unit to be considered for listing.
•WCT are a monophyletic lineage that has been
evolutionary isolated for 1-2 million years.
•There are many non-hybridized populations
remaining.
•Inclusion of hybrid swarms in listing unit will
protect source of ongoing hybridization and
accelerate genomic extinction.
Hybrids sometimes should be part of
the listing unit under the ESA
(2010)
Federal Bison Herds
Cattle
Introgression?
These markers could be used to detect recent
hybridization and to reduce its effect on
conservation herds by removing specific
individual bison from an existing herd, or for
selecting non-introgressed individuals for
translocation.
Hybridized fish have greatly reduced fitness in the wild.
Estimated individual
admixture and number of
progeny produced over a
five year period with 16
microsatellite loci.
Langford Creek
Female fitness
~50% reduction in fitness
WCT females produced ~14X progeny than RT
Male fitness
~50% reduction in fitness
Why is hybridization spreading so rapidly if
the hybrids have such reduced fitness?
(1) Heterosis
(2) “Genomic ratchet” effect
(3) Spatial sorting
First-generation hybrids
Sheltering of deleterious recessive alleles in
first-generation hybrids can increase effective rate
of gene flow and cause loss of local adaptations.
“Genomic Ratchet”
… parental taxa will trend toward extinction as
introgression proceeds in spite of even a heavy fitness
penalty for the hybrids.
Epifanio and Philipp (2001)
• All progeny of hybrid will be hybrids.
• Frequency of hybrids within a population may increase
even when most of the hybrid progeny do not survive.
Consider a population of grey duck hybridizing
with mallards. Assume that we start with 90%
grey and 10% mallards that mate at random, and
the fitness of the hybrids is reduced by t.
That is, the fitness of the grey ducks is 1 and the
fitness of the hybrids is 1 – t.
(Fitness of the mallards is irrelevant since they are
so rare; 1% after panmixia.)
Grey
duck
Gen
0
90%
1
81%
2
66%
3
43%
4
19%
5
3%
Mallard
hybrid
or
10%
Genomic ratchet
t = reduction
in fitness of
hybrids
The proportion of hybrids increases rapidly even
if they have greatly reduced fitness (25%).
Hybridization would spread if
hybrid fish are much more likely to
disperse into other streams than
native fish.
The increase in genotypes at
expanding range edges because of
the increased probability of
dispersal has been termed “spatial
sorting”, and has been proposed to
explain the evolution of fastdispersing individuals at invasion
fronts.
Hybrids are more
likely to disperse
to other streams
Spatial sorting
Thank you!
(n = 7)
(n = 3,150)
Admixture
proportions for
each chromosome
based on 362
mapped SNP loci
Meadow (0.037)
Nicola (0.014)
Admixture proportion
Thank you!
Episodic selection: local adaptations
essential during periodic episodes of
extreme environmental conditions (e.g.,
winter storms, drought, or fire).
Wiens, J. A. 1977. On competition and variable
environments. American Scientist 65:591-597.
Cherry
orchard
After
severe
winter
storm
Deadhorse Creek
Before fire
After fire