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."