mtDNA

Bornean and Sumatran orangutans are the most highly divergent subspecies within any of the living species of great apes. The two farther apart even than chimpanzees and bonobos, which are good biological species. The time of the Bornean-Sumatran orangutan divergence as estimated from mtDNA is around 3.5 million years ago.

This is old enough that many primatologists consider the two populations as separate biological species. The species distinction is supported by some aspects of morphology, but as yet we have no good nuclear DNA information about the extent of divergence. In chimpanzees, nuclear genetic comparisons suggest a relatively recent founding of one subspecies and recurrent gene flow between the others, despite high mtDNA divergence between the subspecies. So information from across the genomes of Bornean and Sumatran orangutans may be necessary to substantiate the hypothesis of long isolation suggested by mtDNA.

Within Borneo, different local populations of orangutans have strong genetic differentiation, with few shared mtDNA haplotypes among them. A new study by Natasha Arora and colleagues [1] has provided further detail about these relationships within Borneo. Based on earlier work, they expected to find high population differentiation within Borneo, and that is what they found:

[O]ur analyses revealed high and significant mitochondrial differentiation, with populations within currently recognized subspecies generally displaying as much differentiation as those between subspecies. Of notable interest is the great extent of subdivision and lack of reciprocal monophyly for the morphologically recognized subspecies P. p. morio and P. p. wurmbii. MtDNA haplotype sharing is uncommon and for populations separated by rivers occurs only in two instances: (i) for SA and GP and (ii) for the northern and southern populations across the Kinabatangan river. In both cases, very recent common ancestry could explain the incomplete mtDNA lineage sorting. For North Kinabatangan (NK) and SK, Jalil et al. (27) proposed an expansion from a recent common refugium further west in Mount Kinabalu, as posited for other Bornean species (46, 47, 49). DV, with its low haplotype diversity, might also be the result of a recent range expansion. GP is located proximally to the Bangka–Belitung–Karimata–Schwaner divide, from where orangutans are presumed to have dispersed to the rest of Borneo (12) and where we might expect a rich haplotype diversity. However, the presence of only one mtDNA haplotype shared with populations further east suggests that the current population in GP is recent and/or underwent a severe recent bottleneck. This and other local bottlenecks make it impossible to reconstruct a colonization of Borneo through the southwestern “choke point” (52).

They were able to confirm the relatively strong differentiation of Bornean populations by examining nuclear microsatellites. These do not give a great indication of the time period over which the populations may have developed their differentiation, but the microsatellites do document the relative lack of allele sharing between the populations, attesting a history of low gene flow in the recent past. The populations they identify as strongly differentiated do not correspond entirely with the subspecies recognized along morphological lines, but there are strongly differentiated populations here.

The "news" aspect of the paper is the one unexpected observation: the mtDNA ancestor of Bornean orangutans lived relatively recently, only around 176,000 years ago (with a range of error stretching from 72,000 to 320,000 years ago. The data in the study do not allow us to distinguish whether this was a time when the Bornean population may have been founded, or whether instead the mtDNA lineage spread through pre-existing populations. The authors pursue the hypothesis that Bornean orangutans were limited to a refugium sometime during the early Late Pleistocene:

Assuming that orangutans arrived in Borneo around the same time as gibbons and macaques, the recent coalescence of Bornean orangutans could be explained by a bottleneck through a severe rainforest contraction. Such a bottleneck would have had a more dramatic impact on the mtDNA structure of orangutans compared with other species as a result of their low densities and slow life histories (18) as well as habitat requirements.

The comparison with gibbons and macaques is necessary because both have substantially deeper mtDNA coalescence times within their Bornean populations. If the forest had been substantially reduced to a small area where orangutans could survive, we might expect the other primates to reflect this event -- and they don't. Nevertheless, a grab-bag of climate change scenarios appear next:

Geomorphological and palynological data indicate the presence of dryer, more open vegetation in southern and western Borneo during the last glaciation (2, 41), and by extrapolation also during other glaciations (but c.f. refs. 42, 43). Climate change was especially severe during an extended cold period within the penultimate glaciation between 130 and 190 ka (44, 45), which occurred approximately at the time of mean coalescence of Bornean mtDNA haplotypes. More recently, the last Toba eruption approximately 74 ka resulted in a short, albeit signi␣cant, decrease in regional temperatures, ensued by a 1,800-y cold stadial (9, 10). Our data do not provide clear signals to make conclusive statements about potential Toba effects. Nonetheless, the coldest period of the penultimate glaciation (44, 45) was more prolonged than the cold period following the last Toba eruption, suggesting more severe effects of the former on the extent of rainforest across Sundaland. In any event, suitable rainforest habitat for orangutans should have existed in certain regions in Borneo where a refugium population survived the dry glacial conditions.

A coalescence time of 176,000 years ago does not point to a short-duration bottleneck that began 74,000 years ago. If orangutans in the Middle Pleistocene of Borneo had high genetic differentiation, a crash would have to have been very severe -- eliminating all but one small regional population -- to have effected the present distribution. Still, the great uncertainty in the actual coalescence time leaves open many possibilities, and the refugium hypothesis in the general case is worth testing, even if the Toba eruption in particular cannot explain the data.

Given the uncertainty about the habitat structure of the now-submerged areas of Sunda, we may also want to consider the hypothesis that the present orangutans arrived recently on Borneo from mainland Southeast Asia. Even if orangutans had lived on Borneo during the Middle Pleistocene, they may not have been the current orangutans. Or even better, they may have been Neanderorangs -- an initial population that was genetically swamped by migrants arriving from elsewhere. The deep Sumatra-Borneo divergence means that the Bornean population was probably not recently derived from Sumatra, but that's a very restricted source compared to the Late Pleistocene distribution of orangutans across mainland and island East and Southeast Asia.

Some other animals walked from Sumatra to Borneo repeatedly during the Pleistocene, including humans. In the human case, we know that a large fraction of the genetic ancestry of Bornean and Javan people was derived from Asia within the last 100,000 years -- in other words, Late Pleistocene gene flow. The movement of genes may have happened in the context of a dispersal of Asian (or ultimately, African-derived) populations into island Southeast Asia. The paper includes some discussion of other primate species:

For instance, the south Bornean gibbon Hylobates albibarbis and the Sumatran–Malaysian gibbon Hylobates agilis have a TMRCA of 1.56 Ma (36), and Bornean and Sumatran pig-tailed macaques have one of 3 to 4 Ma (37). By contrast, the Bornean–Sumatran common ancestor of both the silvered langur(39) and clouded leopard (40) is much more recent than that of orangutans, gibbons, and pig-tailed macaques, probably because of a higher ␣exibility in habitat use.

The pig-tailed macaque divergence time is more or less the same as the orangutan divergence; the others are more like the time range for human dispersals into island Southeast Asia. We can add to the primates a few other medium-sized mammals; for example, clouded leopards are highly differentiated between Sumatran and Bornean populations, and their mtDNA divergence occurred sometime after 3 million years ago.

There may be no contradiction between the recent mtDNA common ancestor and the high degree of population structure in Bornean orangutans; the mtDNA could have been selected. We really would want resequencing of a lot more loci in these orangtuan populations, for which we may not have to wait too long. Mitochondrial DNA is convenient in many ways, including its greater sensitivity to restricted population size and higher mutation rate. But the intrinsic variance of a single gene system under genetic drift is so high that this disadvantage probably outweighs all advantages for reconstructing population sizes.

At any rate, the orangutans now provide an additional case where the subspecies-level history of hominoids is more complex than depicted five or six years ago. Uncovering these kinds of dynamics highlights the need for better modeling of demography and dispersal within a geographically widespread species. Isolation-by-distance and long-lasting subspecies are well-defined models, but when they are refuted, we have a lack of well-defined alternatives.

References

I've written about the study of selection on human mtDNA many times, and discussed the signs that Neandertal mtDNA may have disappeared because of selection.

I love how larger samples are starting to get zoologists to test the neutral hypothesis much more widely. This week, a new paper in Biology Letters by Andrew Foote and colleagues [1] shows that different populations of killer whales. They find possible evidence for positive selection on amino acid-coding variants in cytochrome b in two Antarctic populations.

Here's the last paragraph of the paper. This isn't totally clear without the context (describing the whale populations) but it gives the best short summary of the complexity that was found.

Based on morphological differences [21] and reciprocal monophyly of the mitogenome sequences [12], it has been suggested that type B and type C are distinct species. Positive selection on the cytochrome b could therefore be caused by adaptive divergence relating to a combination of variables that influence metabolic requirements, such as body size or diet; type C is a fish-eating dwarf form of killer whale, whereas type B is one of the largest forms of killer whale and primarily feeds upon seals [21,22] (J. W. Durban & R. L. Pitman 2010, unpublished data). However, the amino acid changes in both ecotypes could be the result of parallel evolution owing to environmental conditions such as oxygen concentration or sea temperature. Both type B and type C at least seasonally inhabit Antarctic pack ice, and both have been sighted over-wintering in the pack ice [21]. The third Antarctic ecotype, for which we found no evidence of positive selection, inhabits the offshore ice-free waters during the austral summer and over-winters at lower latitudes [21]. However, the mutations are in the opposite direction for each ecotype, suggesting that divergent evolution may be more likely. The two changes were private alleles within type B and type C, respectively, and neither substitution was found in the reconstructed ancestral sequence (electronic supplementary material), suggesting that each mutation has occurred and become fixed and almost fixed, respectively, since type B and type C diverged from their most recent common ancestor, approximately 0.15 Ma [12]. Therefore, the ancestral form may not have been subject to the same selective pressures.

Some thoughts:

1. We know how well "reciprocal monophyly" has turned out for human and Neandertal mtDNA genomes...

2. It's interesting how much play there seems to be in the mitochondrial genome. Lots of ways to change and have small phenotypic effects that may be adaptive in one or another ecology. The system as a whole is relatively robust to many mtDNA changes.

3. Many years ago, whale mtDNA was being explained in very similar ways to humans -- a matter of small effective size, in this case exacerbated by matrilineal pod structure. Might well be for many kinds of whales, but selection makes the story more complex.

References