Download - The coastal California Gnatcatcher controversy and how we determine distinctness of biological units
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The coastal California Gnatcatcher controversy and how we determine
dis6nctness of biological units
John McCormack & James Maley Moore Lab of Zoology
Occidental College
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We need sound science influencing land use policy
Ideally we’d base our decisions on science and
try to avoid litigation
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But how do scien6sts determine the basic units of biodiversity?
• We use natural history collections
• We describe and analyze variation within and between populations
• Using both genetics & appearance
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FAQ: Why do you have to have so many of the same species?
Curators get this question a lot
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FAQ: Why do you have to have so many of the same species?
The reason is that if you just had one from each of
two populations, they might look different …
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FAQ: Why do you have to have so many of the same species?
But as you add specimens, you might find those
differences span the range of variation of each
population
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FAQ: Why do you have to have so many of the same species?
Or you might find that the variation doesn’t overlap
at all*
*These represent extremes and it
is possible to detect significant
differences even when the values overlap some
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FAQ: Why do you have to have so many of the same species?
Now imagine comparing many populations and
considering variation by sex and age --- you need a
lot of individuals to conduct a good study on
the units of biodiversity
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The gnatcatcher controversy is a rare moment for
taxonomy in the limelight
Usually this only happens when a new species is
described, like the recent Perijá Tapaculo (Scytalopus
perijanus)
[Avendaño et al. 2015 Auk 132: 450]
Photo: USFWS
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Talk Outline
• coastal California Gnatcatchers
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Talk Outline
• coastal California Gnatcatchers
• Recommendations for describing subspecies
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Talk Outline
• coastal California Gnatcatchers
• Recommendations for describing subspecies
• Why philosophical debates in taxonomy matter to YOU
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What is a “coastal” California Gnatcatcher?
It is the northern subspecies, designated as Threatened under the Endangered Species Act in 1993 based on distinct appearance &
taxonomic status as a subspecies
Polioptila californica californica
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What is a “coastal” California Gnatcatcher?
It is the northern subspecies, designated as Threatened under the Endangered Species Act in 1993 based on distinct appearance &
taxonomic status as a subspecies
Polioptila californica californica Critical habitat
Patchy habitat in SoCal in coastal sage
scrub
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There have been lots of eyes on this taxonomic issue
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There have been lots of eyes on this taxonomic issue
For example Alden Miller, Director MVZ
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There have been lots of eyes on this taxonomic issue
For example Alden Miller, Director MVZ
Dividing line generally set around
the 30 degree parallel
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Your eyes on the problem
Photos courtesy of Phil Unitt at SDNHM
Thanks to natural history collections, you can see for yourself
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Your eyes on the problem
Photos courtesy of Phil Unitt at SDNHM and Jen Gee
Thanks to natural history collections, you can see for yourself
californica has less white in the tail
And a darker back
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From appearance to DNA
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From appearance to DNA
ATTGCTAGGTAGGG
ATTGCTAGGTAGGG
ATTACTAGGCAGGG
ATTACTAGGCAGGG
ATTACTAGGTAGGG
A stretch of DNA with individuals sharing some
mutations
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From appearance to DNA
ATTGCTAGGTAGGG
ATTGCTAGGTAGGG
ATTACTAGGCAGGG
ATTACTAGGCAGGG
ATTACTAGGTAGGG
You can generate a theory of
relatedness between groups and mark
where the changes occurred
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From appearance to DNA
ATTGCTAGGTAGGG
ATTGCTAGGTAGGG
ATTACTAGGCAGGG
ATTACTAGGCAGGG
ATTACTAGGTAGGG
Sometimes the genetic groups are coincident with geographic
areas
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From appearance to DNA
ATTGCTAGGTAGGG
ATTGCTAGGTAGGG
ATTACTAGGCAGGG
ATTACTAGGCAGGG
ATTACTAGGTAGGG
As with appearance, you can still detect differences among
populations even when populations contain mixes of genetic types
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From appearance to DNA
is to as is to
DNA has allowed new insight into evolutionary history, but this shouldn’t mean that we denigrate studies of appearance.
They are looking at two different kinds of variation --- one largely “neutral” and one potentially adaptive.
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From appearance to DNA
And often appearance and DNA corroborate the same story (though there are many exceptions)
Brown et al. 2007
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Gene6cs of the gnatcatchers
• Zink et al. 2000 looked at 1 mtDNA locus
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Gene6cs of the gnatcatchers
• Zink et al. 2000 looked at 1 mtDNA locus
• 1 DNA type (allele) was widespread
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Gene6cs of the gnatcatchers
• Zink et al. 2000 looked at 1 mtDNA locus
• 1 DNA type (allele) was widespread
• Rare alleles found in the south
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Gene6cs of the gnatcatchers
• Zink et al. 2000 looked at 1 mtDNA locus
• 1 DNA type (allele) was widespread
• Rare alleles found in the south
• Petition to delist in 2010 rejected
• USFWS asked for nuclear markers with high mutation rates
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New study, new markers
• Added 8 nuclear DNA regions • Added one more mtDNA region
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New study, new markers
• Added 8 nuclear DNA regions • Added one more mtDNA region
• Added ecological climate modeling
– Using temperature and rainfall data
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New study, new markers
• Added 8 nuclear DNA regions • Added one more mtDNA region
• Added ecological climate modeling
– Using temperature and rainfall data
• Conclusions
– No genetic differences – No ecological differences
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Nuclear markers – the wrong ones Given what was already known from mtDNA, no
one would recommend looking at nuclear DNA loci at this taxonomic level --- not even Zink himself
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Nuclear markers – the wrong ones Given what was already known from mtDNA, no
one would recommend looking at nuclear DNA loci at this taxonomic level --- not even Zink himself
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There were no sta6s6cal tests for divergence
• They eyeballed the geographic distributions of alleles looking for expected patterns
For one DNA region
Drawn from Zink’s 42-page comment to USFWS
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There were no sta6s6cal tests for divergence
• They eyeballed the geographic distributions of alleles looking for expected patterns
Different DNA types & their relatedness Geographical location
of these types
For one DNA region
Drawn from Zink’s 42-page comment to USFWS
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There were no sta6s6cal tests for divergence
Different DNA types & their relatedness Geographical location
of these types
For one DNA region
Drawn from Zink’s 42-page comment to USFWS
• They eyeballed the geographic distributions of alleles looking for expected patterns
• Very qualitative
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There were no sta6s6cal tests for divergence
Different DNA types & their relatedness Geographical location
of these types
For one DNA region
Drawn from Zink’s 42-page comment to USFWS
• They eyeballed the geographic distributions of alleles looking for expected patterns
• Very qualitative • Also the “expected
pattern” is wholly unrealistic – More on this later
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There were no sta6s6cal tests for divergence
Different DNA types & their relatedness Geographical location
of these types
For one DNA region
Drawn from Zink’s 42-page comment to USFWS
• They eyeballed the geographic distributions of alleles looking for expected patterns
• Very qualitative • Also the “expected
pattern” is wholly unrealistic – More on this later
Actual expected pattern from Zink’s comment to USFWS
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• Last summer, a new petition to delist the gnatcatcher from the ESA was filed by the Pacific Legal Foundation
• Reported in a story in the L.A. Times
• 190,000 acres potentially at stake (per L.A. Times)
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In response to the story, and because I
had reviewed the study carefully, I
wrote a letter to the L.A. Times arguing that Zink et al. 2013
was not based on modern methods and
had little chance of finding differences
given their choice of markers and
ecological variables
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This was headline writer’s word choice. I called the science second-rate, not
shoddy.
In response to the story, and because I
had reviewed the study carefully, I
wrote a letter to the L.A. Times arguing that Zink et al. 2013
was not based on the latest methods and had little chance of finding differences
given their choice of markers and
ecological variables
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Zink and Barrowclough wrote
a reply letter
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The editor of The Auk asked me to write a rebuttal paper
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The editor of The Auk asked me to write a rebuttal paper
It was published in January with co-
author James Maley
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The editor of The Auk asked me to write a rebuttal paper
It was published in January with co-
author James Maley
Free open access: http://www.bioone.org/doi/pdf/10.1642/AUK-14-184.1
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Another look at the gene6c data in Zink et al. 2013
• In addition to critiquing marker choice & their sweeping conclusions based on negative evidence
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Another look at the gene6c data in Zink et al. 2013
• In addition to critiquing marker choice & their sweeping conclusions based on negative evidence
• We conducted statistical tests (AMOVA) of the most simple hypothesis – californica is different from south
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Another look at the gene6c data in Zink et al. 2013
• In addition to critiquing marker choice & their sweeping conclusions based on negative evidence
• We conducted statistical tests (AMOVA) of the most simple hypothesis – californica is different from the rest
• We did this because several loci showed private alleles in californica and frequency differences from south
Private alleles
Red allele more
common
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Another look at the gene6c data in Zink et al. 2013
• In addition to critiquing marker choice & their sweeping conclusions based on negative evidence
• We conducted statistical tests (AMOVA) of the most simple hypothesis – californica is different from the rest
• We did this because several loci showed private alleles in californica and frequency differences from south
• AMOVA tests indicated 2 of 7 loci significantly differentiated between coastal CA gnatcatcher and south
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Climate models use environmental data + species occurrence points to predict occupied habitats on a map
Digging into the ecological results
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Climate models use environmental data + species occurrence points to predict occupied habitats on a map
Digging into the ecological results
Environmental data comes from weather
stations and is interpolated over entire
globe
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Climate models use environmental data + species occurrence points to predict occupied habitats on a map
Digging into the ecological results
Environmental data comes from weather
stations and is interpolated over entire
globe
Climate models overlap little between
coastals (gray) and south (black)
from Zink et al. 2013
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Climate models use environmental data + species occurrence points to predict occupied habitats on a map
Digging into the ecological results
Environmental data comes from weather
stations and is interpolated over entire
globe
Climate models overlap little between
coastals (gray) and south (black)
So, different climates
--- but is this interesting?
from Zink et al. 2013
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Let’s imagine a landscape spanning some geographic distance
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N
Let’s call this north --- and we all know it’s generally hotter to the south
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N
In the north the same trees you find at lower elevation…
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N
… are found at higher elevation to the south
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N
Now we can look at birds distributed over this gradient
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N
We can take GPS points of birds from one area
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Temperature
Ra
infa
ll N
Extract the climate data
and plot them
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Temperature
Ra
infa
ll N
And do the same for the
birds from the other
area
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Temperature
Ra
infa
ll N
Gee, look, they are
different. The thing is…
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Temperature
Ra
infa
ll N
If you took GPS points from some rocks in the
areas…
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Temperature
Ra
infa
ll N
And plotted them, they’d
look different too!
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Temperature
Ra
infa
ll N
So how do we know these
differences
are important to the birds?
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Temperature
Ra
infa
ll N
What we can do is take
many random
points from each area
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Temperature
Ra
infa
ll N
And plot those
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Temperature
Ra
infa
ll N
And ask: given what is
available, are the birds in
different habitats?
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Temperature
Ra
infa
ll N
Despite desert being available, maybe birds to the south aren’t
found in the desert
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Temperature
Ra
infa
ll N
Despite desert being available, maybe birds to the south aren’t
found in the desert
Instead they are found in forest, like
the birds in the north
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Temperature
Ra
infa
ll N
Despite desert being available, maybe birds to the south aren’t
found in the desert
Instead they are found in forest, like
the birds in the north
This is called a conserved niche
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Temperature
Ra
infa
ll N
Or maybe similar habitats
are available, but the birds
are in different habitats
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Temperature
Ra
infa
ll N
Or maybe similar habitats
are available, but the birds
are in different habitats
Birds in south in desert despite
similar forest being available
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Temperature
Ra
infa
ll N
Or maybe similar habitats
are available, but the birds
are in different habitats
This is called a divergent niche
Birds in south in desert despite
similar forest being available
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Temperature
Ra
infa
ll N
Finally, you could fail to
reject the null hypothesis
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Temperature
Ra
infa
ll N
Finally, you could fail to
reject the null hypothesis
And find that the birds are in habitats
that are about as different as the general regions where they live
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Temperature
Ra
infa
ll N
Finally, you could fail to
reject the null hypothesis
And find that the birds are in habitats
that are about as different as the
regions where they live
In this case, you can’t disentangle whether the differences in their climate are truly important to the birds or whether it’s
just a trivial effect of living in different places
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Temperature
Ra
infa
ll N
This latter case is what
Zink et al. 2013 found
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Temperature
Ra
infa
ll N
This latter case is what
Zink et al. 2013 found
They failed to reject the null
hypothesis
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Temperature
Ra
infa
ll N
This latter case is what
Zink et al. 2013 found
They failed to reject the null
hypothesis
Yet drew the sweeping conclusion that this meant the gnatcatchers are habitat generalists, which is
unsupported by their results
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The differences in habitat between gnatcatchers is obvious
Coastal sage scrub
Cactus fields
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Vegetation data can be obtained from remote sensing satellites
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You don’t have to work at JPL to get these vegetation layers. You just have to care about looking everywhere you can for
differences.
Vegetation data can be obtained from remote sensing satellites
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Talk Outline
• Recommendations for describing subspecies
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How should we collect gene6c data? We are in a time of incredible new DNA sequencing
technology
We don’t have to rely on 8 DNA regions.
We can collect thousands.
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We finally have gene6c techniques to probe the subspecies level
• Wilson’s Warblers • With mtDNA & other
nuclear loci only east and west distinct
Ruegg et al. 2014
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We finally have gene6c techniques to probe the subspecies level
• Wilson’s Warblers • With mtDNA & other
nuclear loci only east and west distinct
• Using 96 SNPs
• Two subspecies in the western US also distinct
Ruegg et al. 2014
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We finally have gene6c techniques to probe the subspecies level
• Wilson’s Warblers • With mtDNA & other
nuclear loci only east and west distinct
• 96 SNPs
• Two subspecies in the western US also distinct
• Other new methods that gather 1000s of DNA regions
• Actually can gather neutral DNA and DNA controlling differences in appearance
Ruegg et al. 2014
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How should we collect ecological data? In this case, there aren’t too many sites, so how about some
good old-fashioned, ecological field work? Or at least include vegetation layers.
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How should we analyze differences in appearance? • We know they look different
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How should we analyze differences in appearance? • We know they look different • They only question is whether those
differences are “discrete”
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How should we analyze differences in appearance? • We know they look different • They only question is whether those
differences are “discrete”
Geographic distance
One smooth transition without discrete units
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How should we analyze differences in appearance? • We know they look different • They only question is whether those
differences are “discrete”
Geographic distance
One biological unit with a transition to another
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How should we analyze differences in appearance? • We know they look different • They only question is whether those
differences are “discrete”
Geographic distance
One biological unit with a transition to another
• We now have great analytical methods for looking at geographic clines and testing their significance
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Finally, the issue of funding source We said: Research should be carried out either free
from conflicts of interest or where such conflicts are
stated openly
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Finally, the issue of funding source We said: Research should be carried out either free
from conflicts of interest or where such conflicts are
stated openly
We know sponsorship bias exists
Source: Wikipedia
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Finally, the issue of funding source We said: Research should be carried out either free
from conflicts of interest or where such conflicts are
stated openly
We know sponsorship bias exists
It is likely subconscious or a form of publication bias Stating conflicts provides context to public, media, and
other scientists --- it does not mean a study is invalid
Source: Wikipedia
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Zink et al. 2013 funding source
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R. Thornton is a co-filer on the delisting petition
L.A. Times article said funding was from developers
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Drawn from Zink’s 42-page comment to USFWS
Zink now denies study was funded by developers
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Drawn from Zink’s 42-page comment to USFWS
Zink now denies study was funded by developers
Who “incorrectly implied” it?
It’s a direct quote in
quote marks from the
L.A. Times article. No
correction has been sought.
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In any event, the fact that Robert Thornton is a lawyer who has defended developers’ interests has been known to Zink at least since 2005 when Thornton organized a conference and invited Zink to speak
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So, if not developers, who did Robert Thornton secure the money from?
Again, conflicts don’t invalidate a study, but stating them openly is the right thing to do. The discrepancies
in the story and lack of transparency don’t instill trust.
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Talk Outline
• Why philosophical debates in taxonomy matter to YOU
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Or why arcane philosophical debates over taxonomy matter to
YOU
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In 2000, John Avise wrote a classic piece on a certain mental malady afflicting
some adherents of the Phylogenetic
Species Concept, called Cladists (big-C)
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Background: We are all liWle-‐c cladists
Willi Hennig
Hennig invented cladistics & now we build the tree of life based on common
ancestors, not general similarity
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Background: We are all liWle-‐c cladists
Clade or monophyletic
group
Willi Hennig
Hennig invented cladistics & now we build the tree of life based on common
ancestors, not general similarity
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Background: We are all liWle-‐c cladists
Hard for the youngsters to believe phylogenies were ever done without cladistics, but apparently blood was spilled in the hallowed halls of our
natural history museums over all this
Images by David Maddison
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Then big-‐C Cladists went off the rails
• “Cladists” now known for extreme views – If it’s not a clade, it
doesn’t exist
– Parsimony rules
– Models suck
Image by Sam Magruder
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Then big-‐C Cladists went off the rails
• “Cladists” now known for extreme views – If it’s not a clade, it
doesn’t exist – Parsimony rules – Models suck
• Obsession with clades fine for defining older taxonomic groups
• Problems arise at and below the level of the species
Image by Sam Magruder
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We don’t expect clades for subspecies
Time
Here’s the process of speciation!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
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We don’t expect clades for subspecies
Time
Some go extinct; others fuse!
Populations split and begin to differ!
They continue to exchange genes!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
Some go extinct; others fuse!
Eventually gene exchange slows!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
Some go extinct; others fuse!
Eventually gene exchange slows!
Then stops!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
Some go extinct; others fuse!
Eventually gene exchange slows!
Then stops!
Far into future, all gene copies differ!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
Some go extinct; others fuse!
Eventually gene exchange slows!
Then stops!
Far into future, all gene copies differ!
Here’s the taxonomy!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
Some go extinct; others fuse!
Eventually gene exchange slows!
Then stops!
Far into future, all gene copies differ!
Most call these
subspecies or populations!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
Some go extinct; others fuse!
Eventually gene exchange slows!
Then stops!
Far into future, all gene copies differ!
Most call these
subspecies or populations!
Debate over when to call species!
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We don’t expect clades for subspecies
Time
Populations split and begin to differ!
They continue to exchange genes!
Some go extinct; others fuse!
Eventually gene exchange slows!
Then stops!
Far into future, all gene copies differ!
Most call these
subspecies or populations!
Debate over when to call species!
Cladist species!
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We don’t expect clades for subspecies
Time
Cladist species!
Returning to Zink’s expected pattern, it’s
the most conservative anyone would apply for
SPECIES --- and would never be expected for subspecies!
Far into future, all gene copies differ!
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What does a Cladist expect to find below the species level?!
Cladist expecta6ons?
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What does a Cladist expect to find below the species level?!
Cladist expecta6ons?
Not sure, but they explicitly don’t consider processes like gene flow, so
this area describing
what’s happening is left blank!
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Cladist expecta6ons?
Maybe they expect this, all neat
and clean?!
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But then wouldn’t they just call these species?!
Cladist expecta6ons?
Maybe they expect this, all neat
and clean?!
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If subspecies are defined by gene flow, can a big-C Cladist even believe in
subspecies?!
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Drawn from Zink’s 42-page comment to USFWS
Take a moment to ponder this as the expected pattern of nuclear DNA loci for subspecies.!
!And what it would mean for defining
units of biodiversity under
the ESA.!
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So you can collect genetic data until the cows come home.
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“Ultimately this will complete the transition [to cladistic thinking] at ‘lower’ taxonomic scales [e.g., subspecies]. Until then the revolution in systematics and classification started by Hennig remains incomplete.” --- Bob Zink 1999
You won’t see the patterns if this is your viewpoint.
So you can collect genetic data until the cows come home.
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If we let Cladists define the taxonomy of the Endangered Species Act…
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If we let Cladists define the taxonomy of the Endangered Species Act…
…Then we really will be Through the Looking Glass.
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Thanks
• Oxy undergrad Emily Ridley
• Kevin Winker and others provided invaluable advice
• Our work was funded by an endowment to Occidental College by the late Robert T. and Margaret C. Moore
Photo courtesy of U.S. Fish & Wildlife Service.
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Further reading • John E. McCormack & James M. Maley 2015 Interpreting negative evidence
with taxonomic and conservation implications: another look at the distinctness of coastal California Gnatcatchers The Auk 132: 380-388 OPEN ACCESS: http://www.bioone.org/doi/pdf/10.1642/AUK-14-184.1
• Michael A. Patten 2015 Subspecies and the philsophy of science The Auk 132: 481-485 OPEN ACCESS: http://www.bioone.org/doi/pdf/10.1642/AUK-15-1.1
• Robert M. Zink et al. 2000 Genetics, taxonomy, and conservation of the threatened California gnatcatcher Conservation Biology 14: 1394-1405 http://onlinelibrary.wiley.com/doi/10.1046/j.1523-1739.2000.99082.x/full
• Robert M. Zink et al. 2013 Phylogeography of the California Gnatcatcher (Polioptila californica) using multilocus DNA sequences and ecological niche modeling: implications for conservation The Auk 130: 449-458 OPEN ACCESS http://www.aoucospubs.org/doi/abs/10.1525/auk.2013.12241
• Ornithological Monographs, No. 67 2010 [The Subspecies Issue] ALL ARTICLES OPEN ACCESS http://aoucospubs.org/doi/book/10.1525/aoum.67