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brief communications
rhesus or cynomolgus macaques successfullyyielded product from both batches. Sequenc-ing and phylogenetic analyses indicate that those for CHAT 6039 were from cynomolgusmacaques (Fig. 1).
chimpanzee cellular components in two OPVCHAT stocks, together with the positive iden- sequences, provides no support for thehypothesis that these materials were responsi- ble for the entry of HIV into humans and the
source of AIDS.
N. Berry*, C. Davis*, A. Jenkins*, D. Wood†,
P. Minor†, G. Schild‡, M. Bottiger§, H.
Holmes*, N. Almond*
Divisions of *Retrovirology and Virology,
Figure 1 Maximum-likelihood phylogenies were estimated for three V3–V5 data sets: HIV-1 sequences from the Democratic Republic of Congo
National Institute for Biological Standards and (423 base pairs), global isolates (426 base pairs), and Congo and global isolates combined (396 base pairs). Given a phylogeny with tips Control, Blanche Lane, South Mimms, Potters Bar, labelled according to subtype, the subtype diversity ratio (SDR) was calculated as the mean path length between tips of the same subtype divid- ed by the mean path length between tips of different subtypes. For the phylogeny of the global isolates, 11 subtypes were allocated according to standard HIV-1 nomenclature7. For the Congo phylogeny, 11 subtypes were allocated so as to minimize the SDR score, using a heuristic opti- §Karolinska Institute, 17177 Stockholm, Sweden mization algorithm. This assignment is that which gives the maximum possible subtype structure for the Congo phylogeny. The global phyloge- 1. Hooper, E. The River: A Journey to the Source of HIV and AIDS ny gave an SDR of 0.33 and the Congo a value of 0.57. The analysis was repeated after removal of the Congo and global sequences previously identified as intersubtype recombinants4,5. Our analysis will only be affected if recombination breakpoints fall within the V3–V5 region, so 2. Garrett, A. J., Dunham, A. & Wood, D. The Lancet 342, 932–933
excluding recombinants changes the SDR only marginally (0.35 for the global phylogeny; 0.58 for the Congo). SDR values were similar when 3. Dickson, D. Nature 407, 117 (2000).
Congo isolates were assigned to different numbers of subtypes (for example, 0.59 and 0.55 in the case of 8 and 14 subtypes, respectively). To 4. Hahn, B., Shaw, G., DeCock, K. & Sharp, P. Science 287, 607–614
assess the significance of the difference between the global and Congo SDRs, we obtained a null distribution by simulating phylogenies under an exponential growth coalescent process inferred from env gene sequences of subtype A (ref. 6), which is common in Africa. The frequency 5. Berry, N. J. et al. J. Hum. Virol. 1, 457–468 (1998).
distribution of minimum SDR values for these simulated phylogenies is shown in blue. Inset: normalized frequency distributions of intrasubtype 6. WHO Network for HIV Isolation and Characterisation AIDS Res. Hum. Retrovir. 10, 1327–1343 (1994).
path lengths (above the line) and intersubtype path lengths (below the line), plotted on the same horizontal scale (0.0–0.8 substitutions per site), 7. Zhu, T. et al. Nature 391, 594–597 (1998).
for the global and Congo phylogenies. See supplementary information for details of trees and phylogenetic methods.
before the vaccination campaign2, supporting mean between-subtype pairwise distance.
Human immunodeficiency virus
a model of ‘natural transfer’ from chim- Phylogeny and the
panzees to humans3. If this timescale is cor- to subtypes by their phylogenetic relationship rect, then the OPV theory remains a viable to global strains, we used a heuristic algo- origin of HIV-1
hypothesis of HIV-1 origins only if the sub- rithm to assign subtypes such that the sub- The origin of human immunodeficiency panzees before their transmission to humans. Congo and global phylogenies differ signifi- virus type 1 (HIV-1) is controversial. We It has been suggested that the distinctive cantly in the SDR statistic, with the former structure of the global group-M tree, which the Democratic Republic of Congo in Africa has been called a ‘starburst’ because of the phylogenetic trees simulated under a model have a quantitatively different phylogenetic apparently simultaneous appearance of viral of exponential population growth6 (Fig. 1; see tree structure from those sampled in other subtypes, is consistent with the transfer of supplementary information). This result is parts of the world. This indicates that the multiple viral lineages from chimpanzees to conservative because the minimum possible structure of HIV-1 phylogenies is the result of humans1. To test this, we analysed partial env ratio value (representing maximum subtype sequences (V3–V5) of 197 HIV-1 isolates structure) was used in the Congo analysis.
human populations alone, and is not due to sampled in 1997 from the Congo4, a likely Furthermore, although subtypes can be clear- multiple cross-species transmission initiated ly identified in the distribution of pairwise distances for the global sequences (Fig. 1, inset), there is much less distinction between plus 223 sequences representing the global intra- and intersubtype comparisons for the HIV-1 (the viruses responsible for the major- diversity of HIV-1 (including all known sub- ity of global AIDS cases) emerged as a result types), reveals comparable genetic diversity in domly chosen Congo sequences, it is difficult of the vaccination of about one million peo- ple, who were largely living in the Congo strains, with many Congo lineages falling belong to the same or to different subtypes.
from 1957–60, with an oral vaccine against basal to the origin of each subtype as current- polio virus that had allegedly been cultured in ly defined by the phylogeny of global strains5.
global phylogenies probably result from dif- chimpanzee kidneys1. This is claimed to have We tested whether the structure of the Congo ferent epidemiological histories. As many phylogeny differed from that of the global Congo strains appear to be basal, we propose panzee simian immunodeficiency virus, the that each global subtype is the result of the diversity ratio (SDR) of the two phylogenies chance exportation of some Congo strains to Conversely, phylogenetic analysis of HIV-1 (Fig.1). This is defined as the ratio of the other geographical regions, thus producing an sequences indicates that group M originated mean within-subtype pairwise distance to the apparent starburst. Such founder effects have NATURE | VOL 410 | 26 APRIL 2001 | 2001 Macmillan Magazines Ltd
brief communications
been proposed to explain the phylogenetically to return to nursing also revert to an arrhyth- distinct subtypes B and E of HIV-1 group M (ref. 2). The observation that many Congo strains fall basal to the global subtypes also each composed initially of 2,000–2,500 for- suggests that previous phylogenetic analysis agers, their queen and young (sib) brood.
has underestimated the number of lineages that pre-date 1957–60, and hence underesti- known to induce behavioural reversion8 , and mated the minimum number of cross-species indeed the division of labour was reorganized transmissions necessary to reconcile the OPV in these colonies: many bees continued to forage, participating in little or no nursing behaviour; some foragers reverted to nursing the Congo are evidence that the claim of the and stopped foraging completely, or almost OPV theory1 that it is “probably the only hypothesis of origin that can readily explain As in typical colonies with young nurses6, the starburst phenomenon” is incorrect. Our brood care in our experimental colonies was results give us no reason to doubt that the last performed around the clock, with no diurnal oscillations (Fig. 1b). The uninterrupted nursing occurred because individual bees had Andrew Rambaut*, David L. Robertson*,
reverted to arrhythmic activity: analysis of Oliver G. Pybus*, Martine Peeters†, Edward
individually tagged reverted nurses (nǃ66) C. Holmes*
revealed that brood care was performed by *Department of Zoology, University of Oxford, South arrhythmic bees nursing day and night, rather Figure 1 Reverted nurses care for brood with no diurnal rhythm.
than by rhythmic bees working in shifts (Fig.
e-mail: Brood care was observed under dim red light (invisible to bees7) 1c). We found that reversion also affected the †Laboratoire Retrovirus, IRD, BP 5045, 34032 every 3 h for three days. Observations of brood care6: six 10-min activity–rest cycle: 21 reverted bees (31.8%) visual scans of individually tagged bees in the vicinity of the brood.
cared for the brood in seven or more consecu- 1. Hooper, E. The River: A Journey to the Source of HIV and AIDS Foraging observations were made as described6. a, Reorganization
tive observations for 21 hours or longer; for- of division of labour in reversion colonies: frequency distributions of agers, in contrast, rest daily for periods of 2. Korber, B. et al. Science 288, 1789–1796 (2000).
brood care differed significantly (chi-square test, P<0.05) for bees 3. Hahn, B., Shaw, G., de Cock, K. M. & Sharp, P. M. Science 287,
never observed foraging (0, left plot), observed foraging once (1, 4. Vidal, N. et al. J. Virol. 74, 10498–10507 (2000).
middle), or observed foraging more than once (>1, right). b, Colo-
basis of this striking natural behavioural plas- 5. Los Alamos National Laboratory HIV Sequence Database, nial analysis. Mean (DŽs.e.) number of brood care events per obser- ticity is unknown. There may be task-depen- vation period during the day (white bars) and night (black bars) (nǃ6 dent changes in a central clock mechanism, 6. Pybus, O. G., Rambaut, A. & Harvey, P. H. Genetics 155,
scans per observation). To test comprehensively for diurnal rhythms, 7. Robertson, D. L. et al. Science 288, 55–57 (2000).
we pooled the data into two half-day categories and compared the clock, or an effect resulting from nursing Supplementary information is available on Nature’s website at
amount of brood-care activity between them; this analysis was behaviour that overrides the clock output. or as paper copy from the London editorial office of repeated for eight different half-day combinations. No behavioural Comparing these possibilities should help to rhythms were detected (P>0.05, chi-square tests with Bonferonni clarify the nature of the cellular and molecu- correction). Results were similar for two other colonies (data not lar4 bases of chronobiological plasticity.
shown). Foragers and reverted nurses did not differ in age Chronobiology
(29.9DŽ0.2 days, nǃ26, and 29.8DŽ0.4, nǃ8, respectively; brood to maturity in all three colonies.
Reversal of honeybee
Pǃ0.76, unpaired t-test). c, Individual analyses. Number of scans
Although we did not test other possible con- with brood care (days double-plotted). Bars at the bottom right show behavioural rhythms
the light–dark regime outside: black, night; white, day). Sixty-six have wider implications, given the conserva- reverted nurses were analysed individually. Y44: example of a bee tion of some molecular components of bio- Adult honeybees have sleep-like states1,2 active around the clock and showing no diurnal rhythm in brood care logical clocks10and of sleep regulation11,12.
(P>0.05; statistical analyses as above); this behaviour was seen in Guy Bloch*, Gene E. Robinson*†
80.3% of reverted nurses. Y4: example of a bee active around the *Department of Entomology, Neuroscience Program, rhythms as they mature4,5. But whereas dis- clock and with a weak diurnal rhythm in brood care (P>0.05); this University of Illinois, 505 South Goodwin Avenue, ruption of our sleep cycles and synchronized behaviour was seen in 15.2% of reverted nurses. W53: one of only internal rhythms may adversely affect our three bees (4.5%) showing clear diurnal rhythms (P<0.05).
physiology and performance3, we show here 1. Kaiser, W. & Steiner-Kaiser, J. Nature 301, 707–709 (1983).
that honeybees can revert to certain arrhyth- nal circadian clock for timing visits to flowers 2. Kaiser, W. J. Comp. Physiol. 163, 565–584 (1988).
3. Turek, F.W. & Zee, P. C. Regulation of Sleep and Circadian Rhythms (Dekker, New York, 1999).
knowledge, this chronobiological plasticity is 4. Toma, D. P., Bloch, G., Moore, D. & Robinson, G.E. Proc. Natl the first example in any animal of a socially their behavioural development, with their Acad. Sci. USA 97, 6914–6919 (2000).
mediated reversal in activity rhythms.
hive-to-field transition being accelerated, 5. Stussi, T. & Harmelin, M. L. C. R. Acad. Sci. Hebd. Seances. Acad. Sci. D 262, 2066–2069 (1966).
6. Moore, D., Angel, J. E., Cheeseman, I. M., Fahrbach, S. E. & changing colony conditions8. We therefore Robinson, G. E. Behav. Ecol. Sociobiol. 43, 147–160 (1998).
iour development process that underlies the investigated whether this plasticity extends to 7. Von Firsch, K. The Dance Language and Orientation of Bees colony’s division of labour. Larvae must be the bees’ behavioural rhythms, focusing on (Harvard University Press, Cambridge, 1967).
8. Huang, Z. Y. & Robinson, G. E. Behav. Ecol. Sociobiol. 39, 147–158
fed around the clock and are ‘nursed’ in the the reversion from foraging to nursing as a hive by young bees (5–15 days old) that work 9. Schulz, D. J. & Robinson, G. E. J. Comp. Physiol. A 184, 481–488
without any overt behavioural rhythms6. At clock. This reversion occurs in response to a severe shortage of nurse bees and is associated 10. Dunlap, J. C. Cell 96, 271–290 (1999).
11. Shaw, P. J., Cirelli, C., Greenspan, R. J. & Tononi, G. Science 287,
begins to forage outside the hive for pollen with changes in exocrine, endocrine and neu- and nectar, an activity that calls for an inter- rochemical processes8,9. Do foragers induced 12. Hendricks, J. C. et al. Neuron 25, 129–138 (2000).
2001 Macmillan Magazines Ltd
NATURE | VOL 410 | 26 APRIL 2001 |


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