Thursday, March 09, 2006

Pleistocene refugia and late speciation: are extant bird species older than we mostly think?

I learnt today that knuckle-walking is painful, despite practice. I learnt that the British dinosaurs manuscript is still not submitted, that Jaime Headden is one of the most hard-working and reliable people on the planet, and that some people should leave well alone on the subject of Loch Ness monsters. I learnt that my review of Newton’s Encyclopedia of Cryptozoology has been published, though not in a form I totally approve of. And after reviewing other people’s manuscripts on Cretaceous birds, I immersed myself in the salamander literature once more (plethodontids and more on olms to come here soon). One thing led to another, and while checking Wolfgang Wüster’s recent publications I came across Wüster et al.’s response to Gosling & Bush – itself a response to an earlier article by Wüster et al. entitled ‘Tracing an invasion: landbridges, refugia, and the phylogeography of the Neotropical rattlesnake’. And so it begins: as we’ll see, it didn’t take long to veer well off target.

Climatic changes affect the distributions of organisms. This assertion is self-evident, not controversial, and indeed observable within a human lifetime. So given that the planet has experienced major fluctuations in climate within the recent geological past, it follows that well-vegetated habitats were fragmented during the dry cycles of the Pleistocene, and that previously contiguous animal populations became divided. For the purposes of this discussion, this fragmentation had two results: (1) that populations became restricted to refugia – that is, islands of surviving forested habitat; and (2) that speciation was encouraged and accelerated during this time (driving so-called Late Pleistocene Origins, and resulting in the LPO model). So that’s the theory: the ‘glacial refugium’ theory (Rand 1948, Stewart & Lister 2001).

I feel that this view of Pleistocene environmental change is logical and, at face value, well supported. It’s become well accepted to the extent that it’s become the stuff we find in textbooks (e.g. Wiens 1991). But interesting things are happening, and it’s after reading the recent papers on rattlesnake phylogeography that I decided to post to my blog on this. First, I went to the bird literature, as there is an awful lot of it on LPO. If you’re most interested in the rattlesnakes, prepare to be disappointed.

As a nerdy teenager reading all I could on animals, the view I grew up with was that extant birds had speciated during the Pleistocene, and that passerines in particular provided excellent support for LPO. Indeed, the LPO hypothesis has been mostly driven by studies on passerine speciation (Brodkorb 1960). However, this view has come under attack. Genetic data on speciation rates in passerines, published within the last 10 or so years, does NOT support the LPO model.

By looking at recently diverged taxa among North American passerine clades (including grackles, tits, parulids, thrashers and icterids), Klicka & Zink (1997) found that genetic divergence rates actually indicated splits rather older than they’d need to be to satisfy the LPO model: on average, the data suggested Late Pliocene divergence times occurring at about 2.5 million years ago. They determined this by assuming molecular clock rates of 2% per million years however, and herein lies the Achilles heel of their study, as there is considerable doubt as to the idea that genetic changes continue at a clock-like rate. They acknowledged this, and only compared taxa thought to have similar mutation rates. Arbogast & Slowinski (1998) produced a rebuttal arguing that the 2% divergence rate was inaccurate and that Klicka & Zink’s speciation dates were therefore erroneous, but reanalysis still didn’t produce inferred speciation rates young enough to satisfy the LPO model (Klicka & Zink 1998). As Klicka & Zink (1997) state ‘These results contradict the expectations of the LPO model. Overall, these data reflect a protracted history of speciation throughout the Pleistocene and Pliocene’ (pp. 1666-1667), and they termed the LPO model ‘a failed paradigm’. Other genetic studies have also found that extant bird species are actually pretty old (e.g. Zink & Slowinski 1995, Avise & Walker 1998, Avise et al. 1998).

This is very interesting from the palaeontological perspective – it means that by far the majority of passerines aren’t modern/Pleistocene novelties, but have actually been around for a while. Indeed the only taxon found by Klicka & Zink (1997) to be a novelty of this sort is the Timberline sparrow* Spizella taverneri: it seems to have diverged from S. breweri about 35,000 years ago.

* By the way America, your sparrows aren’t sparrows at all, but buntings. That’s a subject for a future blog.

What do the fossils say about this? Well that’s an interesting question, as different palaeornithologists have held conflicting perspectives on this issue. Taken at face value, the fossil record seems mostly to support the LPO model, given that Pleistocene bird fossils are unique to the Pleistocene. Brodkorb (1960) concluded that this was for real, and that few bird species crossed the end-Pleistocene boundary (yes yes, I know we’re still in the Pleistocene, but bear with me here).

Conversely though, others have argued that Pleistocene ‘species’ aren’t demonstrably distinct from Holocene ones – they might only be given different species name because of convention. A review of Pleistocene ‘species’ from Europe showed that the characters used to differentiate Pleistocene ‘species’ from modern ones were mostly vague and unsatisfactory assertions about size or robustness (Stewart 2002). One of the most important factors resulting in the recognition of a new Pleistocene taxon proved to be its age.. yes, that’s right: because it was from the Pleistocene, it must have been a new species. However, this is perhaps an unduly negative view. Tyrberg (2002) found that ‘few, if any, avian species are of Late Pleistocene age [DN: meaning that they’re older] while at least half of the extant Palearctic bird species have their origins in the Pliocene’ (p. 281). If he’s right, then the fossil data is in agreement with what the molecular workers report, and we should not be surprised when extant species are reported from the Pliocene, as they sometimes are.

But – hold on – extant species haven’t just been reported from the Pliocene, but also from the Miocene. Should we be taking this seriously too? Tyrberg (2002) reminds us of the case of Archaeotrogon venustus, an archaeotrogonid that persists in the fossil record for something like 14 million years. Assuming that all the fossils identified as belonging to this species really do represent the same animal (see previous blog on cryptic diversity), this is the longest range recorded for a bird. It indicates that ‘reports of extant species in the Late Miocene should not be rejected out of hand as is usually done’ (Tyrberg 2002, p. 287).

Now, this makes things even more interesting. I’m thinking New Guinea. Why? Many bird genera there – particularly paradisaeids and ptilonorhynchids – have bizarre disjunct distributions. The three similar Paradisaea species P. rubra, P. guilielmi and P. decora are found in the Moluccas (to the west of New Guinea) and in extreme eastern New Guinea, but nowhere in between. The similar astrapia species Astrapia nigra and A. rothschildi live in the Arfak and Tamrau mountains (to the extreme west) and on the Huon Peninsula (to the extreme east), respectively. How can these disjunct distributions be explained? Heads (2001a) argued that the birds must be the products of vicariance: the areas where they occur were formerly close, but as the microterranes moved, the birds have simply been ultra-sedentary and gone with them.

While there are very good reasons for thinking that these birds really are this sedentary (while many birds are great at dispersing, a great many others simply aren’t [Diamond 1981]), I used to think that this just couldn’t be right as there was no way the bird genera, let alone the species, could possibly be old enough. Well, now I’m not so sure. The key tectonic events seem to have occurred in the Miocene, and Heads concluded that the original non-disjunct distribution of the birds must really have dated from this time. Passerines aren’t the only New Guinean taxa with these distributions by the way – it’s present in plants and other groups too (Heads 2001a, b, c, d, 2002).

My plan originally was to discuss how Neotropical rattlesnake phylogeography has actually supported the concept of glacial refugia (that’ll have to be Part II: a post to come in future), then to go from there to the proposed Pleistocene fragmentation of Amazonia. But because birds don’t support the LPO model, they have ended up providing no support for this model, and in fact work on the timing of avian speciation has gone hand-in-hand with criticisms of the refugium theory.

So that’s the ‘bird’s-eye view’ of the area. The ‘rattlesnake’s-eye view’ is somewhat different, and that, as I said, will have to come in another post. For the latest news on Tetrapod Zoology do go here.

The picture above is from here.

Refs - -

Arbogast, B. S. & Slowinski, J. B. 1998. Pleistocene speciation and the mitochondrial DNA clock. Science 282, 1955a.

Avise, J. C. & Walker, D. 1998. Pleistocene phylogeographic effects on avian populations and the speciation process. Proceedings of the Royal Society of London B 265, 457-463.

- . , Walker, D. & Johns, G. C. 1998. Speciation durations and Pleistocene effects on vertebrate phylogeography. Proceedings of the Royal Society of London B 265, 1707-1712.

Brodkorb, P. 1960. How many bird species have existed? Bulletin of the Florida State Museum, Biological Sciences 5 (3), 41-56.

Diamond, J. 1981. Flightlessness and fear of flying in island species. Nature 293, 507-508.

Heads, M. 2001a. Birds of paradise, biogeography and ecology in New Guinea: a review. Journal of Biogeography 28, 893-925.

- . 2001b. Birds of paradise (Paradisaeidae) and bowerbirds (Ptilonorhynchidae): regional levels of biodiversity and terrane tectonics in New Guinea. Journal of Zoology 255, 331-339.

- . 2001c. Regional patterns of biodiversity in New Guinea plants. Botanical Journal of the Linnean Society 136, 67-73.

- . 2001d. Birds of paradise, vicariance biogeography and terrane tectonics in New Guinea. Journal of Biogeography 29, 261-283.

- . 2002. Regional patterns of biodiversity in New Guinea animals. Journal of Biogeography 29, 285-294.

Klicka, J. & Zink, R. M. 1997. The importance of recent ice ages in speciation: a failed paradigm. Science 277, 1666-1669.

- . & Zink, R. M. 1998. Pleistocene speciation and the mitochondrial DNA clock: response to Arbogast & Slowinski. Science 282, 1955a.

Rand, A. L. 1948. Glaciation, an isolating factor in speciation. Evolution 2, 314-321.

Stewart, J. R. 2002. The evidence for the timing of speciation of modern continental birds and the taxonomic ambiguity of the Quaternary fossil record. In Zhou, Z. & Zhang, F. (eds). Proceedings of the 5th Symposium of the Society of Avian Paleontology and Evolution. Science Press (Beijing), pp. 259-280.

- . & Lister, A. M. 2001. Cryptic northern refugia and the origins of the modern biota. Trends in Ecology & Evolution 16, 608-613.

Tyrberg, T. 2002. Avian species turnover and species longevity in the Pleistocene of the Palearctic. In Zhou, Z. & Zhang, F. (eds). Proceedings of the 5th Symposium of the Society of Avian Paleontology and Evolution. Science Press (Beijing), pp. 281-289.

Wiens, J. A. 1991. Evolurionary biogeography. In Brooke, M. & Birkhead, T. (eds) The Cambridge Encyclopedia of Ornithology. Cambridge University Press (Cambridge), pp. 156-161.

Zink, R. M. & Slowinski, J. B. 1995. Evidence from molecular systematics for decreased avian diversification in the Pleistocene Epoch. Proceedings of the National Academy of Sciences 92, 5832-5835.


Anonymous Anonymous said...

Excellent blog, with many nice articles that I have enjoyed reading. However, I have to disagree on the distributions of the two bird genera mentioned in this article as they are neither strange nor disjunct. I can only say that I hope Heads articles (which I haven't read) included better examples. First, members of the Paradisaea are found throughout most of the region (discouting the highest mountain peaks) and only appear disjunct when including the few species that are found the furthest from each other. Virtually all regions in between the three Paradisea spp. mentioned here are inhabited by other species of the genus; that is P. minor of NW and N. New Guinea, P. apoda of SW New Guinea, P. raggiana of E. New Guinea and the aberrant-looking P. rudolphi of the highlands in E. New Guinea. Thus, if going north of the central New Guinea mountain chain the areas between P. rubra and P. guilielmi are "covered" by P. minor, while the areas between P. guilielmi and P. decora are "covered" by P. raggiana. If going south of the central New Guinea mountain chain, P. decora and P. rubra are "connected" by P. raggiana and P. apoda.

The case for the genus Astrapia is similar, though the members of this genus, contrary to Paradisaea, essentially are restricted to the highest mountains. A. rothschildi on the Huon Peninsula Mts. (NE Papua New Guinea), A. stephaniae on the Eastern and Central Highlands (E. and C. Papua New Guinea), A. mayeri on the west-central highlands (WC Papua New Guinea), A. splendidissima on Snow and Starr mts. (C. West Papua in Indonesia) and finally A. nigra of the Huon Peninsula (NW West Papua in Indonesia). Thus, the genus includes 5 para- or allopatric species; one on each major mountain in New Guinea.

12:16 AM  
Blogger Darren Naish said...

Thanks indeed for your comment and the compliment – shame you didn’t leave your name! Anyway, on Heads’ article about the biogeography of birds of paradise etc., I’m afraid you’ve missed the main point. He does indeed (see Heads 2001d) provide a great deal more examples than just species of Paradisaea and Astrapia, discussing in depth the distribution of species and subspecies belonging to Macgregoria, Lycocorax, Manucodia, Paradigalla, Parotia, Pteridophora, Ptiloris, Lophorina, Epimachus, Drepanornis, Cicinnurus, Semioptera and Seleucidis.

While it is true that, among those few species with disjunct distributions that I mentioned (e.g. Paradisaea rubra and P. guilielmi), there are other members of the same genus that ‘bridge the gap’ between the ranges of these species, the point is that the relevant disjunct taxa are sister taxa. So the significance of Paradisaea rubra and P. guilielmi and their disjunct distribution is that they are each other’s closest relatives – never mind the fact that there are other Paradisaea species that occur elsewhere in New Guinea.

This is also true for the other taxa regarded by Heads as revealing disjunct distribution patterns: based on phylogenetic studies (predominantly those of Frith & Beehler (1998) and Cracraft (1992)) he was interested in the distribution of sister taxa. The big surprise is that many sister taxa do not have adjacent allopatric ranges – they have widely disjunct allopatric ranges.

Refs - -

Cracraft, J. 1992. The species of birds-of-paradise (Paradisaeidae): applying the phylogenetic species concept to a complex pattern of diversification. Cladistics 8, 1-43.

Frith, C. B. & Beehler, B. M. 1998. Birds of Paradise. Oxford University Press, Oxford.

9:32 PM  
Anonymous Anonymous said...

Much of Heads criticism of molecular work is based on the argument that the molecular clock relies on calibrations: e.g fossil evidience or geological events, that is, a 'phylogenetic' rate of evolution.

Evidence is mounting (Ho et al. Molecular Biol and Evolution: 2005)that molecular rates of evolution (clock rates) are up to tenfold faster (based on ancient DNA work in birds: penguins, and pedigree studies) than 'phylogenetic' rates (see Penny Nature 2005: Relativity for molecular clocks). This would place many of the bird speciation events you mention well within the Pleistocene.

10:06 PM  
Blogger Darren Naish said...

Thanks for the comment. This is, however, definitely the very last anonymous post that I'm allowing on the site.

10:12 PM  

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