Proposal (388) to South American Classification Committee
Split Diomedea exulans into four species
Effect on SACC: This would divide an existing species, Diomedea
exulans (Wandering Albatross), into four species, at least three of which
have been recorded in South American waters.
Background: The Wandering Albatross (Diomedea exulans) as currently defined
by SACC consists of four taxa:
(1)
nominate exulans (Linnaeus, 1758) of
circumpolar distribution across the Southern Ocean (e.g. South Georgia, Kerguelen,
Heard, Macquarie),
(2) dabbenena (Mathews, 1929) from the
temperate-zone island group of Tristan da Cunha and Gough,
(3) antipodensis (Robertson & Warham
1992) from the sub-polar Antipodes and Campbell Islands off New Zealand,
(4) gibsoni (Robertson & Warham 1992)
from the sub-polar Auckland Islands off New Zealand.
The four taxa are characterized by a
trend of neoteny and decreasing size towards the north, with an all-white adult
plumage in the circumpolar exulans
giving way to a complex pattern of brown immature plumage retention in the
temperate and New Zealand taxa. The morphological distinctness between the two
New Zealand taxa gibsoni and antipodensis is in question, and many
adult individuals cannot be unequivocally identified, although adult gibsoni is generally paler (=less
neotenous) and somewhat approaches exulans
(Tickell 2000; Brooke 2004; Onley and Scofield 2007).
In 1983, a fifth taxon was described
from the temperate Indian Ocean island of Amsterdam (Roux et al. 1983). This
new taxon – breeding at equal latitudes as dabbenena – displays the most extreme form of neoteny with an
all-brown adult plumage. Therefore, Roux et al. (1983) decided to award it
species status: D. amsterdamensis.
However, this treatment is not universally accepted, and some authors have
proposed the inclusion of D.
amsterdamensis in D. exulans
(e.g. Penhallurick and Wink 2004).
New Information: In a controversial book chapter, Robertson and Nunn (1998) put forth a
revised albatross taxonomy in which they elevated all nominal subspecies to
species rank. Consequently, they recognized five Wandering Albatross species.
Their proposal was only partly based on published phylogenetic evidence and was
therefore rejected by some subsequent authors (e.g. Penhallurick and Wink 2004;
Christidis and Boles 2008). However, despite widespread criticism in scientific
circles, the new Robertson and Nunn classification has been widely adopted by
authors of popular bird books (Tickell 2000; Brooke 2004; Onley and Scofield
2007) and by the conservation community (e.g. Birdlife International).
Penhallurick and Wink (2004)
employed GenBank sequences of albatrosses and other seabirds to construct
phylogenetic trees and to compute cyt-b divergences. They found divergences
between the five Wandering Albatross taxa to be well below their 3.2% cut-off
for species status and concluded that all five taxa be lumped into a single
species. Penhallurick and Winks (2004) work came under criticism for
analytical flaws and the rigid use of cyt-b divergences as a species threshold
(Rheindt and Austin 2005).
Burg and Croxall (2004) examined
sequences of the mitochondrial control region in four Wandering Albatross taxa
(exulans, antipodensis, gibsoni,
dabbenena). They found that exulans,
dabbenena, and a clade comprising the two New Zealand taxa (gibsoni and antipodensis) were separated from one another by 4.5 – 5.2%
divergence. The New Zealand taxa gibsoni
and antipodensis were little
differentiated between each other and shared several haplotypes, although there
was one near-fixed difference. Additionally, Burg and Croxall (2004) analyzed
nine microsatellite loci in most samples. They were unable to detect
differentiation between any of their exulans
populations, even between individuals from different oceans, while there were
significant levels of population differentiation between antipodensis and gibsoni.
Based on their genetic data, Burg and Croxall (2004) proposed a three-species
treatment under which the taxon gibsoni
is subsumed under D. antipodensis,
while D. dabbenena and a monotypic D. exulans are also viewed as distinct
species. Please note that Burg and Croxall (2004) did not address P. (e.) amsterdamensis.
Burg and Croxalls (2004) results
agree with phylogenetic studies on other Antarctic sub-polar seabirds that have
demonstrated strong latitudinal differentiation in the absence of longitudinal
differentiation. For instance, Jouventin et al. (2006) detected pronounced
phylogenetic differences in rockhopper penguins and elevated the northern taxon
from the temperate zone to species level (Eudyptes
moseleyi), even though geographic distances between some northern and
southern populations are much smaller than towards their conspecifics. This
finding suggests that global sea currents of different temperature play an
important role in seabird speciation.
Analysis and Recommendation: The biological species status of the five Wandering taxa must be
assessed in the light of two types of considerations:
(1) The relevance of sequence divergence: A vast and growing body of
literature shows that many avian biological sister species are generally
differentiated by at least c. 2-3%
divergence in a number of widely used mitochondrial coding genes (ND2, cyt-b,
COI), although this figure can be substantially lower on account of rapid
speciation (Johnson and Cicero 2004) or can be skewed by genetic introgression
following hybridization (e.g. Funk and Omland 2003). Albatrosses in general and
the five Wandering taxa in particular are characterized by low divergences
(<1% cyt-b; Penhallurick and Wink 2004). These minute values led
Penhallurick and Wink (2004) to unite the five taxa into a single species.
Although Burg and Croxall (2004) found c.
5% divergence between Wandering taxa in the mitochondrial control region, this
locus is known to evolve much faster than the widely used coding genes (ND2,
COI, cyt-b) and, therefore, cannot be compared.
The use of mtDNA divergences as a
species indicator intersects the barcoding debate and the molecular clock debate,
and remains controversial. The latest studies seem to show that a homogeneous
rate of c. 2.1% mtDNA divergence per
million years may apply across a wide range of bird families for comparisons
below the genus level (e.g. Weir and Schluter 2008). This would indicate that
Wandering taxa are very young. However, important differences between rates of
mtDNA evolution among bird families cannot be ruled out (Pereira and Baker
2006) and have even been detected within the Procellariiformes (Nunn and
Stanley 1998).
There are other aquatic bird clades
characterized by tiny interspecific mtDNA divergences (e.g. Anas ducks – Johnson and Sorenson
1999; Larus gulls – Liebers et
al. 2004) possibly related to frequent hybridization and mtDNA introgression in
these groups. Therefore, past introgression events may have artificially
reduced divergences between Wandering taxa and may explain why some researchers
perceive these divergences to be too low for the generally high level of
morphological differentiation.
On the other hand, Friesen et al.
(2007) have shown that speciation in pelagic seabirds may proceed at a much
faster time scale than in most other tetrapods. Their demonstration that a
speciation event between two biological species of storm-petrel dates back only
110,000 – 180,000 years opens up the possibility that the Wandering taxa
may also have attained biological species status in a shorter timeframe than
generally expected.
In summary, tiny mtDNA divergences
among Wandering taxa may be an artifact of introgression. Even if not, the
potentially young age of Wandering taxa does not rule out biological species
status, because even more rapid speciation has been documented in other
seabirds. Therefore, other data sources must be consulted to obtain evidence for
or against the biological species status of Wandering taxa.
(2) The question of taxon allopatry: Akin to Proposal 166 on Shy
Albatrosses, it is relevant to examine whether the Wandering taxa are
allopatric in essence. One sub-polar taxon (exulans)
stretches around the globe and closely approaches the range of the other three
taxa at its breeding colonies in Macquarie Island (620 km to nearest gibsoni, 700 km to nearest antipodensis) and South Georgia (2500 km
to nearest dabbenena). In contrast,
the Atlantic breeding colonies of exulans
(South Georgia) are 5100 km removed from the nearest colony in the Indian Ocean
(Prince Edward Island), and the minimum distance between its Indian Ocean
breeding grounds at Kerguelen and its New Zealand colony at Macquarie is 5800
km. Although Macquarie was not
sampled by Burg and Croxall (2004), their microsatellite data show a panmictic
population structure of exulans
between South Georgia and Crozet across 6000 km. The uniform plumage reflects this lack of genetic differentiation
across the range of exulans and
contrasts with the distinct neotenous adult plumages of the other taxa.
The lack of genetic data on
Macquarie notwithstanding, the small exulans
colony on this island only numbers c.
10 birds and is subject to current immigration and emigration to/from the
Indian Ocean (de la Mare and Kerry 1994). It can, therefore, not be very
different from Indian Ocean colonies in terms of population genetics. In fact, exulans is a widespread visitor to New Zealand and Australian
waters in numbers that exceed the size of the Macquarie colony. The fact that exulans has colonized an island within
the range of gibsoni and antipodensis, but fails to interbreed
with them, suggests that they may have attained prezygotic isolation mechanisms.
Recommendations: Based on the above
considerations, I suggest the following three options for treatment:
(1) One species: Lump all five taxa into D. exulans. This is the status quo, although I am not sure about
SACCs current stance on the extralimital taxon amsterdamensis.
(2) Four species: Recognize all taxa as distinct species, except for gibsoni, which is retained in D. antipodensis. This is Burg and
Croxalls (2004) proposal, though – here again – they did not
comment on amsterdamensis.
(3) Five species: Recognize all taxa as distinct species. This is Robertson
and Nunns (1998) treatment.
I advise against Option 3, because gibsoni and antipodensis are poorly differentiated morphologically and
genetically (Burg and Croxall 2004). The significant microsatellite structure
between both taxa is consistent with subspecies treatment.
As far as Options 1 and 2 are
concerned, I do not feel that there is overwhelming evidence for either
treatment. However, if I were forced to make a recommendation, I would advocate
Option 2, because distributional data indicate that the New Zealand taxa dont
interbreed with exulans even though
they could. By yardstick analogy, the temperate-zone dabbenena (which may have a different life-history owing to its
warm-current environment) would be at the species level because its
control-region differentiation towards the other taxa is even more pronounced
than that of the New Zealand clade (Burg and Croxall 2004). Data on the
extralimital amsterdamensis are
lacking, but on account of its high level of morphological differentiation
(=extreme neoteny) it may be best to go with the describers recommendation for
species status (Roux et al. 1983) until and unless other data have been
presented.
Literature Cited:
Brooke M (2004) Albatrosses and
Petrels across the World. Oxford University Press.
Burg TM, Croxall JP (2004) Global population
structure and taxonomy of the wandering albatross species complex.
Mol. Ecol. 13, 2345–2355.
Christidis L, Boles WE (2008) Systematics and Taxonomy of Australian Birds.
CSIRO Publishing, Canberra.
de la Mare WK, Kerry KR (1994) Population dynamics of the Wandering
Albatross (Diomedea exulans) on
Macquarie Island and the effects of mortality from longline fishing. Polar
Biology 14, 231-241.
Friesen VL, Smith AL, Gmez-Daz E, Bolton M,
Furness RW, Gonzlez-Sols J, Monteiro LR (2007)
Sympatric speciation by allochrony in a seabird. Proc. Natl. Acad. Sci. U S A 104, 18589–18594.
Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly:
Frequency, Causes, and Consequences, with Insights from Animal Mitochondrial
DNA. Annual Review of Ecology, Evolution and Systematics 34, 397-423.
Johnson NK, Cicero C (2004) New mitochondrial DNA data affirm the
importance
of Pleistocene speciation in North American birds. Evolution 58, 1122–1130.
Johnson, K.J. & M.D. Sorenson. 1999. Phylogeny and biogeography of the
dabbling ducks (Genus: Anas): A comparison of molecular and
morphological evidence. Auk 116: 792-805.
Jouventin P, Cuthbert RJ, Ottvall R (2006) Genetic isolation and divergence in sexual traits: evidence for the northern rockhopper penguin Eudyptes moseleyi being a sibling species. Mol. Ecol. 15 (11), 3413-3423.
Liebers
D, de Knijff P, Helbig AJ (2004) The herring gull complex is not a ring species.
Proc. R. Soc. Lond. B 271, 893–901.
Nunn GB, Stanley SE (1998) Body size effects
and rates of cytochrome b evolution in tube-nosed seabirds. Mol. Biol. Evol.
15:1360-1371.
Onley D, Scofield P (2007) Albatrosses, Petrels and Shearwaters of the
World. Princeton University Press, Princeton.
Penhallurick
J, Wink M (2004) Analysis of the
taxonomy and nomenclature of the Procellariiformes based on complete nucleotide
sequences of the mitochondrial cytochrome b gene. Emu 104, 125-147.
Pereira SL, Baker AJ (2006) A mitogenomics timescale for birds detects
variable phylogenetic rates of molecular evolution and refutes the standard
molecular clock. Mol Biol Evol 23, 1731-1740.
Rheindt FE, Austin J (2005) Major analytical
and conceptual shortcomings in a recent taxonomic revision of the
Procellariiformes - A reply to Penhallurick and Wink (2004). Emu 105: 181–186.
Robertson CJR
, Nunn
GB (1998) Towards a new taxonomy
for albatrosses. Pages 13-19 in
Albatross Biology and Conservation. G. Robertson and R. Gales, Eds. Surrey
Beatty, Chipping Norton.
Roux JP,
Jouventin P, Mougin JL, Stahl JC, Weimerskirch H (1983) Un nouvel albatros Diomedea amsterdamensis n. sp. decouvert
sur L'ile Amsterdam (3750'S, 7735'E). Oiseau et la Revue Francaise
d'Ornithologie 53 (1), 1-11.
Tickell
WLN (2000) Albatrosses. Yale University Press, New
Haven, Connecticut.
Weir JT, Schluter, D (2008) Calibrating the
avian molecular
clock. Mol.
Ecol. 17, 2321–2328.
Frank Rheindt, January 2009
Remsen
addendum: Thus a YES vote would indicate favoring a four species treatment, and no
would favor single species (status quo).
If you favor a 5-way split, then vote YES on this one, indicate that you
would favor 5, and if there is enough support, Ill create a new proposal to go
from 4 to 5 species.
Comments
from Robbins: YES, given the current
state of knowledge, Franks suggestion of recognizing four species seems the best course of
action.
Comments
from Zimmer: YES. I find the Burg &
Croxall (2004) proposal to be the most compelling. I cant support treating gibsoni/antipodensis
as separate species, and based on current evidence, Im willing to give amsterdamensis the benefit of the doubt.
Comments from Jaramillo: YES – This is a subject I have been following for a while, and
certainly the treatment of polytypic Wandering, and a separate Amsterdam didnt
jive with me. Certainly if Amsterdam was a species, the other group that shows
considerable neoteny in plumage, particularly that of females (the NZ group, gibsoni and antipodensis) seemed to warrant species status too, for example.
The issue of latitude and water temperature is indeed of considerable importance
in the argument to separate these taxa, and fortunately it is finally being
given the consideration it deserves. We think it logical to separate closely
related yet different (voice, display, morphology, genetics) species east of
the Andes and west of the Andes, well the same is true of temperate vs.
Subantarctic seabirds, water temperature differences may be a barrier as great
as a mountain range or broad river to a landbird. I have not seen any work that
analyzes the displays of these different forms. It would be nice to have that data to work with as well, but
alas it is not out there in a manner that we can use to assess behavioral
barriers to reproduction. But as the proposal states, the potential for mixing
is there, because many of these forms overlap in the broad sense that the at
sea range may include breeding islands of members of other taxa in the complex.
Finally, it may not sit well with some people that some of these taxa are
extremely similar to each other, or even possibly unidentifiable other than at
the breeding island (at least some individuals of the population); however.
this is common in Procellariiformes. Divergence in plumage coloration is not
great in seabirds, and sometimes within-species plumage variation is greater
than between-species plumage variation (observed in various polymorphic Pterodroma, or even Leachs
Storm-Petrel). Four species seems like a reasonable course of events. Although
there are some clear differences between gibsoni
and antipodensis, there are also
greater similarities between these two than with the rest.
Finally,
three of the four have occurred within our waters:
exulans broadly in the southern oceans; antipodensis off Chile (photos and
satellite tracked individuals); dabbenena
in Argentina – Uruguay and I assume Brazil.
Comments
from Pacheco:
"YES. Diante do exposto, eu creio que o
melhor arranjo seja aquele que contempla a adoo de 4 espcies, tal qual
recomendado por Burg e Croxall (2004).
Comments
from John Penhallurick:
Frank Rheindt discusses the taxonomy of five taxa, four of which
(nominate exulans, dabbenena, antipodensis and gibsoni)
have been traditionally treated as subspecies of Diomedea exulans; and one (amsterdamensis)
which was originally described as a separate species (Roux et al. 1983), but
which a number of recent publications (Bourne, 1989; Vuilleumier et al. 1992;
Dickinson, 2003; Penhallurick and Wink, 2004; Christidis and Boles 2008) have
treated as a subspecies of D. exulans. Rheindt appears to recommend
recognising four species: exulans, dabbenena, antipodensis (including gibsoni)
and amsterdamensis.
Rheindt writes relatively approvingly of Robertson and Nunn (1998), who
announced that all terminal albatross taxa (monotypic species and what had
previously been considered subspecies) should be considered species in terms of
the Phylogenetic Species Concept (PSC), to which they indicated their
allegiance. He notes that the
Robertson and Nunn classification has been widely adopted by authors of
popular bird books (Tickell 2000; Brooke, 2004 Onley and Scofield 2005) and by
the conservation community (Birdlife International). It should be remembered that Robertson and Nunns treatment
was published as an unrefereed book chapter, not in a refereed journal. Furthermore, Robertson and Nunn adduced
no evidence at all in support of their proposal: it was simply a matter of fiat in terms of the PSC.
Rheindt also writes approvingly of Burg and Croxall (2004), and notes
that his final preference, that is, recognising four species, agrees with Burg
and Croxalls conclusion. It must
be remembered that both papers by Burg and Croxall (2001, 2004) wrote not in
terms of the multidimensional Biological Species Concept (BSC Mayr 1996). In
terms of what species concept they were using, Burg and Croxall cite Moritz
(1994a and 1994b), who described the differences between management units (MU)
and evolutionary significant units (ESU): ESUs are two groups that show
reciprocal monophyly of mtDNA haplotypes and significant differences in allele
frequencies at nuclear loci. MUs
on the other hand show significant differences in allele frequencies without
regard to the phylogeny of the markers.
They also cite Avise & Wollenberg (1997), who endorsed the
Phylogenetic Species Concept (PSC), which emphasizes the criteria of
phylogenetic relationships, and not reproductive relationships. Thus it appears
that they are using either the ESU model, which stresses conservation values,
or the PSC, which treats all subspecies as good species. Burg & Croxalls discussion is
irrelevant to any discussion of albatross taxonomy in terms of the
multidimensional BSC.
It should be remembered that many recently discussions of albatross
taxonomy have widely relied on conservation values. This is understandable: there are severe threats to many
albatross taxa from practices like long-line fishing. It is extremely regrettable that much conservation
legislation is written in terms of species, not subspecies, the latter of which,
being geographical representatives of species, are often at risk. As Schodde and Mason (1999) have
stated: subspecies, as genetically distinct regional populations, are the
building blocks of evolution and the real units of biodiversity, andmany
more of them are and endangered than biological species. Schodde and Mason
proposed a new term ultrataxon to refer to all terminal taxa, the second
reason for doing so being that it averts a re-circumscribing of Australian bird
fauna under alternative definitions of species, which would lead to ambiguity
and confusion in classification.
However, in the body of their book, Schodde and Mason continued to
classify birds in terms of species and subspecies in the fashion of the
multidimensional BSC.
Rheindt, correctly, recognises the role of neoteny in the
differentiation of these taxa, although it is unclear exactly what he means
when he cites dabbenena as displaying
the most extreme form of neoteny. The plumage of gibsoni, antipodensis and
amsterdamensis recalls stages 1-3 of
nominate exulans. Such changes
probably reflect epigenetic change, and specifically gene silencing, in that
the one or more of the genes that are responsible for the change from juvenile
or immature plumage are switched off. Neoteny is also apparently responsible
for the differences between the two taxa in Diomedea
epomophora, in that sanfordi
retains black upperwings. The juvenile stages of both taxa appear to be almost
identical, involving some black speckling on the back, slightly more in sanfordi, and largely black upperwings;
the nominate shows more white, although the juvenile sanfordi also shows fine white fringing to greater median and some
lesser secondary coverts (Marchant & Higgins 1990: 282). The fact that the cytochrome-b Tamura-Nei distance between these two
taxa is 0.0000% suggests that they diverged very recently. This suggests that the epigenetic
factors involved in such plumage differences can evolve very quickly indeed,
and morphological differences due to such factors should not, of themselves, be
claimed as evidence of species status.
In their critique of Penhallurick and Wink (2004), Rheindt and Austin
(2005) cite specifically Abbott and Double (2003 a, b) as well as Burg and
Croxall (2001,2004) as studies that have uncovered new evidence for the species
status of at least some of these forms.
I have explained above why I do not consider Burg and Croxalls papers
as relevant to the question of species concepts under the multidimensional BSC.
Similarly I do not believe that anything in Abbott and Doubles two papers is
relevant to the question we address here: should a number of taxa traditionally
treated as subspecies within a single species be treated as comprising two or
more species. Of critical
importance in this discussion are the species concepts utilised in these
studies.
Abbott and Double (2003a) initially stated that they were adopting the
species nomenclature suggested by Robertson & Nunn (1998). Since Robertson and Nunn (1998)
explicitly said that they were working within the Phylogenetic Species Concept,
and since Robertson and Nunns paper was not published in a refereed journal,
this is not a promising beginning for any discussion in accordance with the
Multidimensional BSC. In their
abstract, Abbott and Double (2003a) stated that their analysis confirmed the
separation of the shy/white-capped pair and the Salvins/Chatham pair but did not provide species-level resolution
(Emphasis added).
An admitted limitation of Penhallurick & Wink (2004) was that it
relied on a single gene: cytochrome-b,
which was criticised by Rheindt and Austin (2005) and also in Rheindts
Proposal 388. And it is obviously
desirable to confirm these findings with studies of other, particularly
nuclear, genes. However, it should
be remembered that many studies have confirmed the utility of both cytochrome-b and Bayesian inference. For example, May-Collado & Agnarsson (2006), in a study of cetacean
phylogeny, stated in their abstract:
Until more genes are available for a high
number of taxa, can we rely on readily available single gene mitochondrial
data? Here, we estimate the phylogeny of 66 cetacean taxa and 24 outgroups
based on Cyt-b sequences. We judge
the reliability of our phylogeny based on the recovery of several deep-level
benchmark clades. A Bayesian phylogenetic analysis recovered all benchmark
clades and for the first time supported Odontoceti monophyly based exclusively
on analysis of a single mitochondrial gene. The results recover the monophyly
of all but one family-level taxa within Cetacea, and most recently proposed
super- and subfamilies. In contrast, parsimony never recovered all benchmark
clades and was sensitive to a priori weighting decisions. These results provide
the most detailed phylogeny of Cetacea to date and highlight the utility of
Bayesian methodology in general, and of Cyt-b
in cetacean phylogenetics. They furthermore suggest that dense taxon sampling,
like dense character sampling, can overcome problems in phylogenetic
reconstruction.
What Penhallurick & Wink (2004) said in
relation to Diomedea exulans and Diomedea epomophora was as follows:
We provide a distance matrix for
albatrosses as Table 2. In the
text that follows, nucleotide distances are given, with amino acid distances
following in brackets. Considering
the distances in the Table 2, those between the species that were split by
Robertson and Nunn (1998) are much smaller than those between previously
recognised "good" species of albatross. For example, within the D.
exulans complex, the distance between Robertson and Nunn's D. chionoptera [= nominate exulans] and D. antipodensis
is 0.52 % (0.00 %); in the case of their D.
exulans [= dabbenena], 0.87 %
(0.00 %); and in the case of gibsoni,
0.52 % (0.00 %). D. gibsoni
shows a percentage difference of 0.00 % (0.00 %) from D. antipodensis and 0.70 % (0.00 %) from dabbenena. Compare
these distances, all of less than 1.0 %, with the distances ranging from 3.2 %
to 3.6 % between both D. e. epomophora
and D. e. sanfordi from all of the taxa in the exulans complex. We
conclude that gibsoni, antipodensis and dabbenena are better recognised as subspecies of D. exulans than as good species in their
own right. We note that in the
case of antipodensis and gibsoni, both were described as a
subspecies of D. exulans in their original description by Robertson and
Warham (1992: 74 and 76).
Somewhat surprising is the distance
evidence relating to D. amsterdamensis,
which has sometimes been treated as a good species since its description by
Roux et al. (1983), although Bourne
(Table 4 1989: 112) treated it as a subspecies of D. exulans. The fact that it is only 0.52 % (0.00 %) distant from antipodensis, gibsoni and exulans, and
only 0.87 % (0.00 %) removed from dabbenena
strongly suggests that it belongs among the subspecies of exulans.
In our unpublished reply to Rheindt and Arndt
(2005), which was, I believe very unfairly, denied publication, we made the
following point:
The Tamura-Nei distance between nominate epomophora and sanfordi is 0.0000%, and the same distance is found between D. e. gibsoni and D. e. antipodensis.
This figure suggests that the divergence between these taxa was very
recent. Whereas Burg and Croxall
(2004), in terms of ESUs, suggested splitting exulans from antipodensis/
gibsoni and both from dabennena,
the TN distances of 0.902% between nominate exulans
and dabbenena; of 0.539% between exulans and antipodensis; of 0.539% between exulans
and gibsoni; of 0.540% between exulans and amsterdamensis; are well below the TN distance between exulans and epomophora of 3.797%.
These data suggest that in terms of the Multidimensional BSC, we have
only two species: D. exulans and D. epomophora, although it would seem
appropriate to class dabbenena as a
semi-species.
On the question of taxon allopatry, Rheindt
concludes The fact that exulans has
colonized an island within the range of gibsoni
and antipodensis, but fails to
interbreed with them, suggests they may
have attained prezygotic isolation mechanisms.(Emphasis added). To claim that
because a small number of birds (ca. 10) on Macquarie Island have failed to
interbreed with birds on islands 620 km north in the case of gibsoni and 700 km north in the case of antipodensis proves or even strongly
suggests that they could never interbreed again stretches the imagination.
Rheindt concludes tiny MtDNA divergences among
Wandering taxa may be an artifact of
introgression(Emphasis added). Introgression refers to the movement of a gene
from one species into the gene pool of another by backcrossing an interspecific
hybrid with one of its parents (Dowling and Secor 1997). It is a long-term process; it may take
many hybrid generations before the backcrossing occurs. Given the extreme philopatry of all
Diomedea albatross taxa, the idea of such lengthy processes of hybridisation,
of which there is no evidence whatsoever, seems implausible. I conclude that
mention of two possibilities, without any evidence for the reality of either,
does not amount to any kind of proof.
In Proposal 388, Rheindt refers to criticism of
Penhallurick and Wink (2004) for rigid use of cyt-b divergence as a species threshold (Rheindt and Austin
2005). Yet Rheindt himself cites
as authoritative a study by Burg and Croxall which appeals to c.5% divergence
between Wandering taxa in the mitochondrial control region, although he
concedes this locus is known to evolve much faster than the widely used coding
genes (ND2, COI, Cyt-b). There is an obvious contradiction here.
Rheindt and Austin (2005) identified several problems under this
heading. Firstly, saturation and
multiple substitutions are a serious problem as one goes deeper in the
phylogeny. I agree. Because of its fast rate of mutation,
cytochrome-b would be unsuitable for
investigating relationships at the order level. But most of the taxonomic issues Penhallurick and Wink were
addressing in their 2004 paper concerned levels of divergence of 5% or
less. And it is highly unlikely
that multiple substitutions, which require two or more changes at a single
site, are going to be a problem at that level. The use of Tamura-Nei weighted distances also reduces
potential saturation problems.
A second problem identified by Rheindt and Austin (2005) is the
difference in rates of molecular evolution among bird lineages. They made the mistake of assuming that
Penhallurick and Wink were applying a universal rate of evolution:
specifically, that we tend to reject separate species status for any taxon
pair with a divergence of <2%.
What we were actually trying to apply was the principle enunciated by
Helbig et al. (2002) in discussing the types of evidence that might be applied
to determine the species status of allopatric taxa. They referred to: DNA sequences, and the sum of the
character differences corresponding to or exceeding the level of divergence seen in related species that coexist in
sympatry. Throughout, when dealing
with possible species, we used the distance between well-established species in
the same group as a measuring stick.
And it was this judgement that guided our decisions on status.
I believe that is both unfair and incorrect of Rheindt
and Arndt (2005) to say that Penhallurick and Wink (2004) propose to once
again revise the albatross taxonomy.
In relation to albatrosses, we supported the analysis contained in Mayr
& Cottrell (1979) and in Marchant & Higgins (1990, vol. 1. Part A:
264-354, except that that source treated the taxon we call dabbenena as the nominate of D.
exulans, and referred to the taxon we call exulans as D. e. chionoptera);
and also in del Hoyo, Elliott and Sargatal (1992); Dickinson (2003) and more
recently Christidis and Boles (2008). Diomedea
exulans gibsoni and Diomedea exulans
antipodensis were both described as a subspecies by Robertson & Warham
(1992). Since Robertson & Nunn (1998) claimed to be relying on genetic
distances, our main concern was to point out that a more reasonable view of
distances supported the traditional analysis.
Finally, I would like to point to a glaring
lack in relation to proposals submitted to the SACC: specifically, the lack of
any criteria for making judgments about whether the difference between taxa
should be at the species or subspecies level. In the absence of such criteria, one does not know how to
evaluate proposals such as 388.
Nowhere in his proposal does Rheindt explicitly state in terms of what
species concepts he is making his proposal. It does not appear to be the
strictest form of the PSC, which views all terminal taxa as species, since he
proposes to treat antipodensis and gibsoni as conspecific. Perhaps he, like
Burg and Croxall, is working in terms of the ESU or MU concepts of Moritz
(1994a and 1994b). But if the multidimensional BSC is at least implicitly the
standard by which such proposals must be judged, I submit that Proposal 388
fails the test.
References
Abbott, C. L. and Double, M. C. (2003a). Phylogeography of shy and
white-capped albatrosses inferred from mitochondrial DNA sequences:
implications for population history and taxonomy. Molecular Ecology 12:
2747-2758.
Abbott, C. L. and Double, M. C. (2003b). Genetic structure, conservation
genetics and evidence of speciation by range expansion in shy and white-capped
albatrosses. Molecular Ecology 12: 2953-2962.
Avise J. C. and Wollenberg, K. (1997). Phylogenetics and the origin of
species. Proceedings of the National
Academy of Sciences of the USA 94:
7748-7755.
Bourne, W. P. (1989) The evolution,
classification and nomenclature of the great albatrosses. Le Gerfaut 79:
105-116.
Burg, T. M. and Croxall, J. P. (2001). Global relationships amongst
black-browed and grey-headed albatrosses: analysis of population structure
using mitochondrial DNA and microsatellites. Molecular Ecology 10:
2647-2660.
Burg, T. M. and Croxall, J. P. (2004). Global population structure and
taxonomy of the wandering albatross species complex. Molecular Ecology 13:
2345-2355.
Christidis, L. and Boles, W. E. (2008). Systematics and Taxonomy of Australian Birds. CSIRO Publishing,
Collingwood, Victoria.
Dickinson, E. C. (2003) The
Complete Howard and Moore Checklist of the Birds of the World. Rev and
enlarged 3rd edn. Princeton University Press, Princeton, New Jersey.
Dowling, T. E. and Secor. C. L. (1997). The role of hybridization and
introgression in the diversification of animals. Annual Review of Ecology and Systematics. 28: 593-619.
Helbig, A. J., Knox, A. G., Parkin, D. T., Sangster, G. and Collinson,
M. (2002) Guidelines for assigning species rank. Ibis 144: 518-525.
del Hoyo, J., Elliott, A. and Sargatal, J. eds. (1992)
Handbook of the Birds of the World,
Vol. 1. Lynx Edicions, Barcelona.
Marchant, S. and Higgins, P. J. (1990) Handbook of Australian, New Zealand and Antarctic Birds. Vol. 1.
Oxford U. P., Melbourne.
May-Collado, L. M. and Agnarsson, I. (2006) Cytochrome
b and Bayesian inference of whale phylogeny Molecular Phylogenetics and Evolution 38, 344-354.
Mayr, E. (1996). What is a species and what is not? Philosophy of Science 63,
262-77.
Mayr, E. and Cottrell, G. W. (1979) 'Checklist of Birds of the World'.
Vol. 1, 2nd edn. Museum of Comparative Zoology, Cambridge, Mass.
Moritz, C. (1994a). Defining evolutionarily significant units for
conservation. Trends in Ecology and
Evolution 9: 373-374.
Moritz, C. (1994b).
Applications of mitochondrial DNA analysis in conservation: a critical review. Molecular Ecology 3: 401–411.
Penhallurick, J. M and Wink, M. (2004) Analysis of the taxonomy and
nomenclature of the Procellariiformes based on complete nucleotide sequences of
the mitochondrial cytochrome-b gene. Emu 104:
125-47.
Rheindt, F. E. & Austin, J. J. (2005) Major analytical and
conceptual shortcomings in a recent revision of the Procellariiformes – a
reply to Penhallurick and Wink (2004). Emu
105: 181-186.
Robertson, C. J. R. and Nunn, G. B. (1998) Towards a new taxonomy for
albatrosses In Albatross biology and
conservation (Eds. G. Robertson and R. Gales) pp. 13-19. Beatty and Sons,
Chipping Norton.
Robertson, C. J. R. and Warham, J. (1992) Nomenclature of the New
Zealand Wandering Albatrosses. Bulletin of the British Ornithologists' Club.
112 (2): 74 - 81.
Roux, J.-P., Jouventin, P., Mougin, J.-L., Stahl, J.-C., and
Weimerskirch, H. (1983) Un nouvel albatros Diomedea
amsterdamensis n. sp. dcouvert sur l'Ile Amsterdam (37o50'S,77o35'E).
Oiseau 53: 1-11.
Schodde, R. and Mason, I. J. (1999) The
directory of Australian birds: passerines. CSIRO Publishing, Collingwood,
Vic.
Vuilleumier, F., Le Croix, M. and Mayr, E.
(1992) New species of birds described from 1981-1990. Bulletin of the British Ornithologists Club, Centenary Supplement,
112A: 267-309.
Rheindts response to the comments by Penhallurick:
Penhalluricks
comments are rather antagonistic and suggest my proposal seeks to establish one
taxonomic treatment of Wandering Albatross at the expense of the other.
However, my main conclusion states that – as far as the 1-species or
4-species solutions are concerned – I do not feel there is
overwhelming evidence for either treatment So essentially, I concur with
Penhallurick to the point that his favored 1-species solution may well turn
out to be the best treatment at some point in the future when more evidence is
available. However, with the current evidence at hand, I believe that the
4-species solution would make more sense within the framework of the Biological
Species Concept, for reasons expounded in the proposal.
In his interpretation
of my proposal, Penhallurick has misunderstood a number of important points and
missed the significance of others. He dwells on particulars of a scientific
debate carried out in the journal Emu in 2004/05 (Penhallurick and Wink 2004;
Rheindt and Austin 2005) that – in my opinion – has only marginal
relevance to the current proposal, resulting in the mix-up of a number of
unrelated issues. For instance, Burg and Croxalls (2004) incidental finding of
5% control region divergence is not the reason why my proposal cites this study
as supporting BSC species status of Wandering taxa. Rather, the phylogenetic
structure these authors found among Wandering taxa is used in conjunction with
ecological observations (range sympatry) to advance this case.
I do wish to offer a
clarification on four central points brought forth by Penhallurick.
(1) Penhallurick asks SACC members to disregard
some of the most pertinent research carried out on Wandering Albatross
systematics because the authors phrased their results under a different species
concept. I believe we should not throw out these detailed studies on Wandering
Albatross phylogenetic structure only because their authors opt to describe
their findings in terms of ESUs rather than biological species. Despite
Penhalluricks concern, SACC members have the ability of re-interpreting those
results under their own species concept.
(2) Similarly, Penhallurick is confused about which
species concept underlies the present proposal. In line with SACCs adoption of
the multi-dimensional BSC, my proposal followed the other 387 SACC proposals in
utilizing this species concept. This is obvious by mention of such terms as
essential allopatry, which would be immaterial to a debate within the confines
of most other species concepts widely used in ornithology.
(3) Penhallurick states that I write approvingly
of Robertson and Nunn (1998) and Burg and Croxall (2004). Apart from being
irrelevant, this is not true. In fact, if anything, I wrote disapprovingly of
Robertson and Nunns (1998) controversial book chapter. Penhallurick then
goes into a lengthy discussion on how the conservation community has welcomed
or pushed the treatment of Wandering taxa as separate species. Here again, I
fail to see the relevance to the current SACC discussion. Just as conservation
concerns should not motivate a split in albatross taxa, the illegitimacy of
this interference should not be used as an argument to motivate a lump.
(4) Most significantly, I take issue with Penhalluricks
portrayal of genetic introgression in albatrosses as an implausible and
lengthy process of hybridization of which there is no evidence whatsoever
Introgression rather than conspecificity as a cause of near-zero mtDNA
divergences among Wandering taxa is not just a theoretical exercise, but also a
plausible scenario. The following
three points are meant to illustrate that genetic introgression is not a
marginal process, but an all-encompassing phenomenon:
a.
MtDNA
introgression is pervasive in the biological world and greatly diminishes the
utility of low mtDNA divergences as a true yardstick of taxon divergence. (Note
that high divergences are less gravely affected). Judging by the inflationary
number of studies reporting on introgression, it seems to occur in most animal
species in one form or the other. In birds alone, patterns of genetic
introgression have been detected across the whole taxonomic spectrum, from
passerines to Galloanseres. A small number of example studies include the
following (full citation not provided): Gill 1997; Brumfield et al. 2001;
Helbig et al. 2001, 2005; Rohwer et al. 2001; Bensch et al. 2002; Stre et al. 2003; Lovette 2004;
Kulikova et al. 2004; Mank et al. 2004; Shapiro et al. 2004; Grant et al. 2004;
Dabrowski et al. 2005; Borge et al. 2005; Secondi et al. 2006; Kvist and Rytknen 2006; Vallender et
al. 2007; Peters et al. 2007; Martnez-Cruz and Godoy 2007; Rheindt et al.
2009; Carling and Brumfield 2008, 2009; Gay et al. 2008.
b.
As pointed
out in the original proposal, mtDNA introgression can affect all/most members
of entire radiations, such as Anas
ducks (Johnson and Sorenson 1999, Peters et al. 2007) and Larus gulls
(Liebers et al. 2004). Plumage differences between various Larus gulls are arguably smaller than between an adult male Snowy
Albatross (D. exulans) and his
neotenous cousin from the north (e.g. D.
amsterdamensis). While introgression is widely accepted as the cause for
near-zero mtDNA divergences in Larus,
why should it not be plausible in Diomedea?
If we were to subscribe to Penhalluricks divergence-only approach, we would
also have to be prepared to challenge the biological species status of Greater
and Lesser Black-backed Gulls based on their near-zero mtDNA divergence
(Liebers et al. 2004).
c.
Penhallurick
paints genetic introgression as a long-term process requiring many generations,
and thus finds it to be an implausible phenomenon in albatrosses.
Penhallurick errs on two accounts. Firstly, genetic introgression can be
extremely fast. For an avian example, take Mank et al.s (2004; Conservation
Genetics 5) research showing how Mottled Duck and Mallard microsatellites went
from distinct to almost identical within only 58 years. Secondly,
Penhalluricks statement belies the vast time scales of the evolutionary
process. Why – in the last tens of thousands of years – could there
not have been, say, a climate-induced 500-year period (or repeated episodes of
such periods) during which exulans
expanded into the ranges of the other Wandering taxa and occasionally
hybridized with them, leading to introgression from one taxon into the other
and a re-setting of mtDNA divergence to zero There is no reason to presume
introgression in Wandering Albatrosses must have happened fast and now.
Based on these considerations,
I re-iterate my view that near-zero mtDNA divergences in Wandering Albatross
taxa may not be too informative to this taxonomic debate, and that other lines
of enquiry (e.g. their essentially sympatric occurrence around New Zealand) may
provide more information on their BSC status.
Comments
from Stiles:
YES. I think that the 4-species treatment is the
best way to express what we know about these birds, and I think that Rheindt
has satisfactorily answered the objections of Penhallurick.
Additional
comments from Penhallurick: Some final comments on
Rheindts Proposal. If we consider
Rheindts proposal, and ignore the appeals to irrelevant papers, the core of
his proposal comes down to two statements of possibilities. He states that introgression may
explain the low DNA distances. He
offers no actual evidence that this has occurred. And he needs to explain not just how introgression occurred
between two Wandering Albatross taxa but between all of them. This beggars the imagination. Secondly, we are invited to assume that
because a small number of exulans are
present on Macquarie Island, this represents breeding isolation between that
taxon and taxa on Subantarctic Islands some 700 km away. Think about this! It
would be laughable in any serious discussion. Again, Rheindt presents no evidence that this most unlikely
convergence ever occurred. I
thought science was about evidence.
And Rheindt has presented none!
Additional
comments from Rheindt: Please see Liebers et al. (2004; Proc. R. Soc. Lond. B) for a
well-documented example of a species swarm of approximately a dozen BSC species
of Larus gull that all share
near-identical mtDNA, presumably as a result of introgression. Similar patterns
(but with less comprehensive documentation) have been detected in Anas duck mtDNA - see previous
contribution. It is questionable why such a pattern should ...beggar
imagination... in albatrosses."
Comments from John Croxall (12 Jan. 2010): I was recently informed of the existence of this proposal
and although I would not normally get involved in such issues, I felt that the
SACC might find a few comments useful to help it reach a decision. (For the
record: (a) I have undertaken
research on albatrosses and petrels for some 30 years to my retirement in
2006; (b) I am not a taxonomist; such work on albatrosses that I have
co-published were by-products of studies on population genetics and parentage
largely conducted by Theresa Burg; (c) I have never met, or refereed
papers by, Rheindt or Penhallurick!).
Additional published
material
There
are at least 4 supplementary sources of information that are relevant to your
deliberations:
1. The very
recent paper (despite its June 2009 date, the issue only appeared in November)
by Chambers et al. (2009) Phylogenetic analysis of the 24 named albatross taxa
based on full mitochondrial cytochrome b
DNA sequences. Notornis 56: 82-94. To me, on a quick perusal (and despite its abundant
typographic errors), this provides a good and pragmatic overview of many of the
issues, not least those involved in considering the approach and conclusions
propounded by Penhallurick and Wink (2004). While the paper does not consider relevant biological
(especially ecological) information (see below), I believe the
essence of its conclusions in respect to the taxa relating to your proposal are
entirely realistic and would support the proposal for splitting. I attach a
copy of the paper.
2. The
paper by Techow et al. (2010) Speciation and phylogeography of giant petrels Macronectes. Molecular Phylogenetics and Evolution 54: 472-487, as this has considerable bearing on the issue of
cytochrome b sequence divergence
(see below). I attach a copy.
3. The
publications of the Taxonomic Working Group of the Agreement on the
Conservation of Albatrosses & Petrels (ACAP), which has reviewed several of
the Diomedea issues relevant to your
proposal, specifically Diomedea
antipodensis and gibsoni at its
2006 meeting and D. exulans and D. amsterdamensis at the 2008
meeting. They have not yet
reviewed D. exulans/D. dabbenena. However, given the principles and
precedents involved and that Burg and Croxall (2004) found there was more genetic
distinction between dabbenena and exulans (sensu stricto) than between exulans
and antipodensis/gibsoni, it would
seem unlikely that the ACAP Taxonomic Working Group would not support this
split (it is the existing ACAP position).
I attach the documents (AC2, AC3, AC4) from to the
relevant meetings of this Working Group; these are available publicly through
the ACAP website. I am not a
member of this Taxonomic Working Group but its discussions are relevant to BirdLife International (see below),
for which I am the ACAP representative to its Advisory Committee and Meeting of
Parties.
4. In
respect of Diomedea dabbenena, the
publication by Cuthbert et al. (2003) Separating the Tristan albatross and the
wandering albatross using morphometric measurements. Waterbirds 26: 338-344,
is also relevant. Tristan
albatross, although showing reasonable genetic divergence, is not easy to
distinguish in the field from D. exulans,
without considerable experience of age and sex-related plumage patterns of the
latter. In essence, their ranges
overlap at sea only in the wintering grounds, particularly in the Brazilian and
Benguela Current systems where Tristan albatross may co-occur with D. exulans from South Georgia towards
the northern limits of the latters wintering range. There are numerous recent
observations and uplinks from tracking studies confirming the regular
occurrence of Tristan albatross in the SACC area.
5. SACC
also raises the issue of D.
amsterdamensis, material of which was unavailable to Burg and Croxall
(2004); some relevant data were provided in Milot et al. (2007) Proc.
Roy. Soc. Lond. Series B 274: 1779-1787 and I understand there is a paper forthcoming which
summarises all data relevant to its distinctiveness at the species level. However this species is, to date,
unrecorded for the SACC area (indeed it has quite a restricted (at all seasons)
main distribution at sea in the Indian Ocean).
Comments on the proposal to
SACC
Background
1. The
statement (New Information para 1) that despite widespread criticism popular
bird books is incorrect. First,
while Penhallurick and Wink (2004) – on rather
tendentious grounds – and Christidis & Boles (2008) – on
grounds which may equally reflect lack of any real experience of the taxa
involved (and both representing at most personal/ regional perspectives on this
complex)- were critical of the adoption of the Diomedea splits, the vast majority of the scientific community
has accepted them, as evidenced by references in the reports of the ACAP
Taxonomic Working Group. Second,
this acceptance extends to recent monographic treatments, e.g. Tickell (2000);
Brooke (2004); Onley and Scofield (2007).
The authors of these works would be somewhat dismayed to be regarded as
non-scientists! Tickell was a
pioneer researcher on albatrosses as long ago as 1958; Brooke has published for
over 20 years on avian ecology, especially with respect to seabirds,
including describing new procellariiform taxa; Scofield is a leading New
Zealand museum-based researcher with wide field experience of albatrosses and
petrels. Thus all recent global
reviews have chosen to maintain most of the splits in Diomedea taxa that are the subject of your proposal.
2. The
BirdLife International position is as follows. As the authority for the IUCN Red List, BirdLife maintains a Taxonomic Working
Group (BTWG). For regions with authoritative
checklist/classification committees, these are very closely followed by BirdLife. However, for taxonomic groups of more global distribution, BirdLife prefers to use the latest
authoritative global review. For
Procellariiformes, the default authority is Brooke (2004), with updates as
determined by BTWG in its annual review process. For albatrosses, however, BirdLife
currently follows the advice of the ACAP Taxonomic
Working Group, regarding this as the most appropriate taxonomic authority for
the species covered by this Agreement.
Sequence
Divergence
1. It is
increasingly recognised that, compared with most avian taxa, Diomedeidae,
probably Procellariidae and possibly Procellariiformes, show unusually low levels of sequence divergence even between
well-established species.
2. This topic
is reviewed and discussed for albatrosses by Milot et al. (2007). The difficulty, of course, is how to
compare distances between taxa that are mainly (indeed entirely for all
problematic cases) allopatric, given the limited guidance available from
congeneric sympatric taxa. For me,
there are two main guidelines here.
First, Black-browed and Campbell Albatross, which now
breed sympatrically at Campbell Island, are separated by 0.8%. Second, the two giant petrels are
separated by about 0.4%. The
latter is quite an important result because we know from extensive (multi-year
of banded individuals) field studies of these cryptic sibling species that
hybridisation is almost non-existent (the few cases are invariably Southern
males with Northern females), especially noteworthy considering that the loose
breeding aggregations of both species often overlap spatially, that the
observable discriminating morphological characteristics are essentially only in
bill colour and that their annual cycles are only staggered temporally by some
5-6 weeks. Everyone who has worked
in the field with these two species where they breed sympatrically recognises
the correctness of their discrimination by Bourne and Warham (1966) as distinct
species. It is remarkable that
Penhallurick and Wink (2004) chose to ignore the wealth of biological and
ecological data on these taxa – literally a dozen or more publications
whereby species distinctiveness had not only never been questioned but
invariably clearly substantiated- in favour of applying some arbitrary genetic
distance standard.
Even recognising that Macronectes is in a different family of the Order, it nevertheless
has many biological and ecological similarities to albatrosses (diurnal,
surface breeders with vocal and plumage characteristics highly conserved), and
emphasises that procellariiform taxa which may look almost identical to us and
which have very low cytochrome b divergence,
may still behave as perfectly good biological species.
This
is not the place to rehearse the arguments for the taxonomic status of the Diomedea and Thalassarche taxa, perhaps beyond recognising that there
are probably three difficult cases, for most of which more data would be
useful:
(a) Diomedea
antipodensis/gibsoni, discussed in some detail by Chambers et al (2009),
where the ACAP TWG decision (in AC2 paper)
was to retain as subspecies, the identical cytochrome b sequences
and limited microsatellite differences finding more favour than the plumage
differences at most ages and the very distinct foraging areas and migrations
outside the breeding season (the former taxon occurring regularly (annually on
migration) in the SACC area; the latter mainly restricted to the Tasman Sea
when not breeding)).
(b) D.
epomophora/sanfordi (both of which occur in the SACC region), whose
distinctive plumages render them diagnosable at almost all ages and stages yet cytochrome b differences are very low (0.08%) and
hybridisation does occur (albeit at the not entirely natural site of Taiaroa
Head). The ACAP TWG addressed this species pair in its AC4 paper and maintained
full species status for both. [For the record, based on my experience with Thalassarche
melanophrys and T. chrysostoma,
hybridisation events can occasionally take place between species which are
as different as these two, if there are mixed colonies with substantially disproportionate numbers
of the two species involved. In Diomedea,
the relatively high frequency of extra-pair copulations, including forced
copulations, may also lead to hybrid pairs at sites where individuals of one
species are sometimes attracted to breeding sites populated by another
species].
(c) Thalassarche cauta and
T. steadi (the latter occurring in the SACC region) which currently lack
100% reliable morphometric or plumage diagnostics for all ages and stages (but
bill colour allows discrimination in almost all cases and breeding seasons
differ by about 8 weeks) and have cytochrome b
distances of about 0.2%. However,
these two taxa have been the subject of a dedicated phylogeographic PhD thesis
and the ACAP Taxonomic Working Group (in its AC3 paper) reached a unanimous
decision based on the published papers there from; consequently BirdLife has followed this decision.
I
do not wish to extend these comments to address issues raised by Penhallurick. However, I would simply observe that,
whatever the merits of the higher order taxonomic and nomenclatural
modifications suggested in the Penhallurick and Wink (2004) paper, over 100
albatross and petrel scientists, meeting at the Fourth International Albatross
and Petrel Conference in Uruguay in 2004, were unanimous in agreeing that most,
if not all, of the conclusions relating to the species status of albatrosses,
giant petrels, and prions were in direct disagreement with the experience of
those scientists who had worked most extensively with these species in the
field. It is evident that the
Penhallurick and Wink (2004) conclusions disregarded the substantial body of
biological and ecological information available on the distinctiveness of most
of the taxa in the above groups, where modern data on genetics, vocalisations,
ecology, core foraging areas etc. are demonstrating the distinctiveness of
these mainly allopatric taxa in ways consistent with their recognition at
species level under all of the currently accepted concepts.
Additional
comments from Robbins:
Given Rheindt and Croxalls comments, I see no
reason to change my original vote of supporting recognition of four species.
Additional comments from Stiles: Here, I merely reiterate my YES vote, especially in view of Croxalls
reply to Penhalluricks latest salvo.
The fact that a group of world experts on the albatrosses has
collectively supported species status for these forms is not to be lightly
dismissed. As a definite
non-expert I am strongly inclined to accept their verdict.
Comments from Schulenberg: YES. As several have
noted, this case is a tough nut to crack, as the biological species concept is
poorly suited to treat essentially allopatric taxa, and other taxonomies are
reasonable. All that said, similar as all these taxa are, I am impressed by the
differences among them, both in terms of genetic structure between populations,
and in terms of trends towards neoteny in plumages (correlated with latitude).
Therefore I think that recognizing four species (including the extralimital amsterdamensis) is the best approach.
Also, while fully aware of the distance between Macquarie Island (breeding site
for exulans) and Campbell and
Auckland islands (breeding sites for antipodensis/gibsoni), I'm more impressed by the
relative proximity of these sites. Low genetic distances notwithstanding, the
morphological and ecological differences point to me towards recognizing these
taxa as species.
The question of English names is not, to my knowledge,
before us. But if SACC accepts the split, then I foresee issues with English
names. The name "Wandering Albatross" has long standing, and maybe
there will be resistance to changing it. But the name "Wandering
Albatross" would prove useful for (the great many) individuals of the
complex (sensu lato) that might not be identifiable in the field. In turn, a
different English name would be called for to use for Diomedea exulans (sensu stricto). Onley and Scofield (2007) use
"Snowy Albatross" for exulans.
I don't think that this has been followed by other authors, but ... they may be
on to something.
Comments from Remsen: NO. My understanding of these albatrosses
is that they will breed in subadult plumages with fully adult-plumaged
individuals. If that is incorrect,
please let me know. If this is
true, then the neotenic plumage differences among island populations seem
unlikely to act as any barrier to gene flow, consistent with the low degrees of
genetic divergence. The
correlation with latitude suggests an ecological response among the populations
rather than any intrinsic biological difference that indicates that they are
lineages that have reached levels of divergence associated with species rank in
other birds. As for differences
among island populations in timing of breeding, migration routes, and wintering
areas, such differences occur among island populations of many seabirds that no
one would consider to consist of multiple species, and are therefore not really
persuasive on their own. To a non-seabird
biologist such as myself, all I see is discrete geographic variation in plumage
characters correlated with an ecological variable. Vocal differences are alluded to, but I would like to see
published data on this. Seabird
biologists working with shearwaters have been tuned in to vocal differences and
their importance for some time, but I am not aware of a parallel emphasis in
albatrosses – if this only reveals my ignorance, someone please correct
me.
Having
discussed species limits with a number of seabird biologists, they have openly
lobbied me for species rank for populations because that would increase
their status in terms of conservation.
Thus, their taxonomy has an agenda, driven by politics, and this arouses
my suspicions. I do not want to
accuse any of the 100 albatross and petrel scientists (mentioned by Croxall) of
such non-scientific, subjective reasoning, but I am concerned that such
reasoning may enter their decision of endorsement of narrower species limits,
if only subconsciously. Id also
like to know how many of them have training in systematics rather than just
ecology. Such comments will
undoubtedly insult this active and extensive community of researchers, but I
only mean to provoke production of the sort of data that will fortify these
taxonomic decisions particularly in this case data on actual isolating
mechanisms (voice and display?).
Finally, I want to emphasize that my vote on this has nothing to do with
degree of genetic (mtDNA) differentiation.
Comments from Cadena: [NO]. I have remained on the sideline regarding this
proposal because I know close to nothing about the biology of these birds and
wanted to have comments from most committee members and others, hoping they
would illustrate me. I am actually uncertain as to how to vote, so
hopefully the following comments will stimulate some additional discussion that
may finally lead us to reach a decision soon. What I see here is that much of
the Rheindt vs. Penhallurick discussion boils down to a rather simple issue:
Rheindt is only saying that there are various reasons why low (or no) mtDNA
differentiation need not imply conspecificity and that because of those reasons
one ought to look at other sources of data to decide how to rank all these
forms. I have to say I agree with Rheindt on this 100%. Then, what else do we
have? I am not certain about all the details, but as Van puts it, the
strongest evidence for splitting these forms are differences in plumage and,
based on his first remark, plumage variation is unlikely to be a barrier to
gene flow (right?). To me, differences in timing of breeding are persuasive
arguments for species status for sympatric populations, but not for populations
existing in allopatry that may be tracking changes in e.g. resource availability
and lack fixed genetic differences in genes controlling breeding behavior, such
that they would mate if they were to come into contact (e.g. Ecuadorian
populations of Zonotrichia capensis
separated by 25 km differ drastically in breeding seasons as a result of
climatic differences between sites, but nobody seems to have claimed these
should be considered different species). Alvaro mentioned differences in water
temperature between sites as a possible isolating factor, but this to me seems
like a difference in the environment, not a difference in the organisms, so
using it as an indication of reproductive isolation (following the BSC) appears
problematic as essentially all biological species show some ecological
discontinuities in their ranges and comprise populations occupying ecologically
different environments (take again the Zonotrichia
case, with populations occurring from sea level to very high-elevation areas).
Is there anything else? If not, I think my vote would lean towards NO. I
realize this might challenge the opinion of albatross experts mentioned in the
proposal, but if these experts were not weighting the evidence for reproductive
isolation following the criteria we try to follow here, then I would be fine
with reaching a different conclusion.
Comments from Nores: NO. Because it depended on my vote whether the Wandering Albatross
were considered 1 or 4 species, I have devoted considerable time to analyze the
fundamentals given by Rheindt, Penhallurick, Croxall, and the other members of
the Committee, supporting one position or another, in order to make a decision.
Although conservation of the species cannot be a reason for analyzing taxonomic
issues, I had initially thought of voting YES because seemed there were good
reasons for either treatment, and an affirmative vote would favor conservation
of the taxa. However, I now
consider that the reasons for keeping all the taxa within a single species are
more important than those for splitting them. I want to make it clear that this
decision does not mean to contradict a number of experts in marine birds
(Tickell, Brooke, Onley, Scofield, Croxall or any of the 100 albatross and
petrel scientists mentioned by the latter) because I believe that this is
ultimately a taxonomic matter rather than one of the biology of the species.
There seem to me to be two fundamental reasons for keeping all the populations
in a single species:
1) Taxa allopatry: the breeding areas of the
five taxa clearly show that all of them are allopatric. D. e. exulans occurs in the southern part
of the species range (Southern
Georgias, Crozet, Kerguelen, Prince Edwards and Macquarie islands), whereas the
all other taxa are to the north: Tristan da Cunha and Gough I. (dabennena), Amsterdam I. (amsterdamensis), Auckland I. (gibsoni) and Antipodes I. (antipodensis) (see Figure), which mated
the typical distribution of subspecies.
The fact that exulans has been breeding in Macquarie Island, 620 km from the
nearest gibsoni and 700 km from the
nearest antipodensis, is not a proof
of sympatry as suggested by Rheindt. This author has also mentioned The fact
that exulans has colonized an island
within the range of gibsoni and antipodensis, but fails to interbreed
with them, suggests they may have
attained prezygotic isolation mechanisms. I agree with Penhallurick that to
claim that a small number of birds (ca. 10) on Macquarie Island having failed
to interbreed with birds on islands 620 km north, in the case of gibsoni, and 700 km north in the case of
antipodensis suggests that they could
never interbreed is seems implausible.
2) Low Molecular divergence: the five Wandering Albatross taxa are characterized by very low
divergences. The Tamura-Nei distance between D. e. gibsoni and D. e.
antipodensis is 0.0000%. The TN distances of 0.902% between nominate exulans and dabennena, of 0.539% between exulans
and antipodensis, of 0.539% between exulans and gibsoni and of 0.540% between exulans
and amsterdamensis are well below the
TN distance between exulans and epomophora of 3.797% These data suggest
that in terms of the Multidimensional BSC, we have only two species: D. exulans and D. epomophora (Comments from Penhallurick). Although Burg and
Croxall (2004) found c. 5% divergence
between Wandering taxa in the mitochondrial control region, this locus is known
to evolve much faster than the widely used coding genes (ND2, COI, cyt-b) and,
therefore, cannot be compared (Comments from Rheindt). Although Rheindt
concluded that tiny MtDNA divergences among Wandering
taxa may be an artifact of introgression
(and he may be correct), he offered no actual evidence that this has
occurred. He only offered examples
in other birds (e.g. Anas ducks
– Johnson and Sorenson 1999; Larus
gulls – Liebers et al. 2004). Moreover, he needs to explain not just how
introgression occurred between two Wandering Albatross taxa but between all of
them.