Proposal (949) to South American Classification Committee

 

 

Treat Caryothraustes brasiliensis as a separate species from C. canadensis

 

Background: The species we treat as Caryothraustes canadensis (Yellow-green Grosbeak) consists of four subspecies (1) simulans of the Darién, extreme e. Panama, (2) nominate canadensis of the Guianan Shield region and other regions locally in northern and eastern Amazonia, (3) frontalis from e. Brazil (Paraíba, Pernambuco, Alagoas), and (4) brasiliensis of southeastern Brazil (Bahia to RdJ).  They differ primarily in head pattern, especially with respect to forehead color, and degree of overall plumage brightness.  They have been treated as a single species, as far as I can find, throughout their history (e.g. Hellmayr 1938, Paynter 1970, Sibley & Monroe 1990, Dickinson & Christidis 2014, etc.).

 

Tangentially, I can’t think of any other species that has such a distribution pattern, at least when you add an isolated population from the Darién– very interesting.

 

New information: Tonetti et al. (2017) analyzed vocal, plumage, morphometric, and genetic data of the three South American subspecies.  They generated maximum-likelihood and Bayesian trees of hypothetical relationships based on mtDNA (ND2; 29 samples; only 1 of simulans but otherwise fairly evenly distributed).  Otherwise, simulans was not included in the quantitative analysis because of lack of access to specimens.  They quantified standard song parameters from 52 recordings, and morphometric and plumage variation (color catalog names) using 163 study skins.

 

They found that that the three South American subspecies are diagnosable units based on coloration, and from photos, also tentatively concluded that isolated simulans is also diagnosable; their two populations of nominate canadensis show some possibly diagnostic color variation that is being further investigated.  Morphometric analyses showed limited variation among the three South American subspecies.  They found no differences in vocalizations: no significant differences were found among them in any of the parameters measured.  The ND2 gene trees produced 4 clades: 2 clades within nominate canadensis; simulans; and frontalis + brasiliensis.  Here’s the Bayesian tree (ML tree had similar topology):

 

 

Things to note: one group of three specimens from nominate canadensis are sister to all samples of the other subspecies as well as the rest of the nominate canadensis samples.  From their table, these three come from a locality in Maranhão and two in Pará, one of which is from the Xingu.  I can’t figure out from their Fig. 4 map where all the other samples come from, and there do not seem to be enough place markers to account for them.  That distant, isolated, trans-Andean simulans falls inside canadensis is curious.  Although frontalis and brasiliensis are diagnosable based on extent of black on forehead color, they are interdigitated in terms of ND2.

 

The authors taxonomic conclusions are that their data support recognition of two species.  Hand-waving about whether oscine song can be used as a taxonomic character evidently is used to dismiss the non-diagnosability in voice.  The genetic data on their own show that canadensis is paraphyletic with respect to brasiliensis, but this is not discussed, or perhaps I am missing where that is discussed.  That there is a 5-6% p-distance between the two populations of canadensis and simulans vs. frontalis or brasiliensis is evidently the primary basis for recognizing two species.

 

Tangent: They recommended synonymizing frontalis with brasiliensis based on lack of diagnosability with respect to mtDNA.  However, frontalis is diagnosable based on plumage, as their data clearly show, so the correct interpretation of their results is that it is a valid taxon (contra those who expect subspecies to be diagnosable on the basis of a few neutral loci).  In fact, that diagnosability was so obvious that in the first draft of this proposal I missed the conclusion of Tonetti et al. that frontalis was not a valid taxon based on lack of reciprocal monophyly.  Rafael Lima (pers. comm.) alerted me to this misinterpretation, and he recently published (Lima 2022) what I would consider the correct interpretation of the data.  With the reasonable assumption that the plumage differences have a genetic basis, I take this opportunity again to point out that recognizing these diagnosable differences taxonomically is important and that lack of geographic structure in patterns of variation of a few neutral loci should not mask these potentially important patterns of phenotypic variation.  See Patten and Remsen (2017) for the full sermon.

 

Discussion: The paper nicely establishes that the four described taxa are diagnosable units and thus valid subspecies.  It also reveals that there may be an undescribed taxon within canadensis based on genetic data that evidently corresponds to some plumage variation (to be investigated).  Although the paper recommends that brasiliensis (including frontalis) be treated as a separate species from canadensis (including simulans) based on ND2 distance data, I am unable to follow completely the logic for that given that the major genetic break, at least using ND2, is between two populations of canadensis, and that using those same genetic data, C. canadensis would be paraphyletic.  Philosophically, I am further opposed to recognizing species-level taxa based on an arbitrary break on the continuum of genetic divergence, especially when based on a single neutral locus.

 

My interpretation of the results is that there is no evidence for treating brasiliensis as a separate species, but rather plenty of evidence, both vocal and genetic, for treating all taxa as a single species under the BSC, with at least four valid subspecies (or PSC species).

 

Recommendation: I recommend a NO vote on this proposal for reasons stated in previous paragraph.

 

Literature cited (other than standard references):

 

Lima, R. D.  2022.  On the validity of Caryothraustes canadensis frontalis (Hellmayr, 1905) (Aves: Cardinalidae).  Zootaxa 5165 (1): 144–150.

Patten, M. A. and J. V. Remsen, Jr.  2017.  Complementary roles of phenotype and genotype in subspecies delimitation.  Journal of Heredity, 2017: 1–3.

TONETTI, V. R., F. BOCALINI, L. F. SILVEIRA, AND G. DEL-RIO.  2017.  Taxonomy and molecular systematics of the Yellow-green Grosbeak Caryothraustes canadensis (Passeriformes: Cardinalidae).  Revista Brasileira de Ornitologia 25: 176–189.

 

 

Van Remsen, June 2022

 

 

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Comments from Robbins: “NO, for reasons outlined in proposal.”

 

Comments from Claramunt: “NO. I agree with Van, I don’t see the evidence for the split in the mtDNA data. At least plumage and mtDNA show conflicting patterns.”

 

Comments from Areta: “NO. Some claims by Tonetti et al. (2017) are perplexing. For example, their proposition to synonymize the diagnostic black-fronted frontalis with brasiliensis based on their lack of reciprocal monophyly in a mitochondrial gene (0.3 p distance), as highlighted by Van and further shown by Lima (2022). The vocal analyses are too coarse-grained to be informative. The phylogenetic relationships must be taken with a grain of salt, given the low support of several clades (e.g., the non-sister relationship of the two Amazonian, phenotypically similar "populations"). However, the deep ND2 genetic divergences among all forms (always above 5.5% for any pair; except for frontalis-brasiliensis) caught my attention and beg for an explanation (as does the low divergence of frontalis-brasiliensis: might this be a case of mitochondrial capture?). A paper by Bocalini et al. in prep is mentioned by Tonetti et al. (2017), which would provide genomic data and presumably more detailed phenotypic characterizations could hold the key to solve the taxonomy of Caryothraustes canadensis. Until then, there are enough uncertainties here as to recommend caution and not adopting any split in the group.”

 

Comments from Stiles: “NO for now, pending the whole-genome analysis of these that is apparently in the works.”

 

Comments from Lane: “NO. For reasons outlined by others, this suggested split lacks important backing to make it seem necessary at this point.”

 

Comments from Rafael Lima: “I have just one more comment about Caryothraustes — I saw that Areta and Stiles mentioned the "Bocalini et al. in prep" paper that was cited by Tonetti et al. (2017). The article in question has already been published:

 

Bocalini, F., Bolívar-Leguizamón, S. D., Silveira, L. F., & Bravo, G. A. (2021). Comparative phylogeographic and demographic analyses reveal a congruent pattern of sister relationships between bird populations of the northern and south-central Atlantic Forest. MPE 154: 106973.

https://doi.org/10.1016/j.ympev.2020.106973 

 

“The results of this paper concerning Caryothraustes may be worth commenting on the proposal, particularly those regarding simulans (which, possibly, may be best treated with C. poliogaster rather than as a member of the C. canadensis complex).”

 

Comments from Bonaccorso: “NO. For the reasons stated in the proposal. For me, it is bizarre that they propose lump simulans into canadensis, regardless of the tree structure (resulting from a neutral marker, but still the only genetic data available).”

 

Comments from Pacheco: “NO. In view of the arguments put forward here, caution is needed when adopting the split.”