Hox Gene Variation and Evolution

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Hox Gene Variation and Evolution news and views annually degasses about 1 gigatonne (109 not nitrate exhaustion. on the microbial algae. The growth perfor- tonnes) of CO2 (ref. 3), equivalent to 20 per Yet the paradox persists. Virtually all phy- mance of the diatoms is all the more surpris- cent of current anthropogenic output. The toplankton species, including the picoplank- ing as nitrate reduction requires energy regression lines and intercepts of dissolved ton, are able to use nitrate; indeed, phyto- and the mediating enzyme contains iron. inorganic carbon, silicate and nitrate con- plankton other than diatoms routinely Indeed, why diatoms can be so much more centrations, measured in the upper 200 m of exhaust nitrate in the surface waters of the efficient than the other algae despite the the EUZ, indicate that silicate availability non-HNLC ocean. So why does this not hap- nitrate handicap needs to be explained. regulates both carbon and nitrate uptake pen in the EUZ and other low-silicate HNLC Balancing pelagic ecosystem budgets is and fate. The slope of the highly significant regions? Differences in grazing pressure still an art because we know so little about the 5 regression between nitrate and silicate is 1, have been proposed as an explanation . One abilities and predilections of the organisms8 which coincides with the known require- widely held view is that the small algae of the and their interactions with one another5. ment of these two elements by diatoms. The microbial loop are kept in check by heavy Whatever the outcome of studies on the lim- intercept represents the excess nitrate (about grazing pressure, whereas diatoms, because iting factors in the various HNLC regions 4 mmol m–3) that confers HNLC status on of their larger size (and possibly also the pro- and their subsystems, the status of diatoms as the EUZ. tection offered by the silica shell), are less key players will not be challenged. The work- Silicate is bound in mineral shells (bio- prone to being grazed by the smaller proto- horses running pelagic systems are recruited genic silica) of no food value. In the EUZ zoa6. So relaxation of a limiting factor (such from this algal group: their new production model, the diatom shells are packaged in as iron) results in accumulation of diatom not only fuels the food chains leading to fish zooplankton faeces and exported wholesale but not picoplankton cells. Whether contin- but also provides the raw material driving from the surface layer. In contrast, nitrogen ued iron fertilization will eventually lead to the biological pump and ultimately the great is selectively retained by the diatom grazers nitrate exhaustion by non-diatom phyto- biogeochemical cycles of the ocean. It is time which, in the course of their metabolism, plankton in low-silicate HNLC regions we gained a better understanding of the excrete ammonia; in turn the ammonia is remains to be tested. properties that make diatoms so special. assimilated by the photosynthesizing cyano- In Dugdale and Wilkerson’s steady-state Victor Smetacek is at the Alfred-Wegener Institute bacteria (<2 mm) and small flagellates (2–10 EUZ model, the biomass-to-production for Polar and Marine Research, Am Handelshafen mm) of the ‘microbial loop’. This ubiquitous ratio of the diatoms indicates that they were 12, 27570 Bremerhaven, Germany. community (pico- and nanoplankton) is growing at least as fast as, if not faster than, e-mail: [email protected] additionally composed of small protozoa the microbial algae. To maintain steady state, 1. Dugdale, R. C. & Wilkerson, F. P. Nature 391, 270–273 (1998). that feed on the minute algae and bacteria, as grazing pressure on the diatoms, presumably 2. Doney, S. C. Nature 389, 905–906 (1997). well as on one another, which also release by copepods (zooplanktonic crustacea, 3. Tans, P. P., Fung, I. Y. & Takahashi, T. Science 247, 1431–1438 ammonia (see Fig. 2 of Dugdale and equipped with mandibles edged with silica (1990). 4. Coale, K. H. et al. Nature 383, 495–501 (1996). Wilkerson’s paper, page 272). The ammonia- the better to crush diatom shells with), must 5. Banse, K. Oceanography 7, 13–20 (1994). based production within this tightly geared have been similar to or even higher than that 6. Banse, K. ICES J. Mar. Sci. 52, 265–277 (1995). community — termed regenerated produc- tion — contributed four-fifths of the total Developmental biology daily production (new plus regenerated) in the EUZ. Because of the low variability Hox gene variation and evolution in nutrient and biomass concentrations Axel Meyer observed over different cruises and seasons, the pelagic system of the EUZ seems to have settled into a steady state which can be oth developmental and evolutionary questioning of this commonly held hypoth- likened to a silicate-limited chemostat. biologists try to explain patterns in the esis — that genomic and morphological The silicate-to-nitrate ratios in the other Bdiversity among organisms, and the complexity are causally linked2–7. HNLC regions — the Southern Ocean and Hox genes encode a class of transcription Using an experimental approach based the subarctic Pacific — are much higher than factors that have provided ample material on the polymerase chain reaction, Prince et in the EUZ, yet fairly similar community for such discussions. Because they may be al. unambiguously identified 34 Hox genes structures, total production rates and ratios pivotal in specifying regional identity in and determined their linkage with somatic- of new-to-regenerated production are rou- body plans, differences in their expression cell hybrids. Surprisingly, they found that tinely measured there. Diatom growth is evi- could (at least partly) explain the evolution the zebrafish has three Hox genes (HoxC3, dently not silicon-limited, so other factors, of animal phyla. The Hox genes are arranged HoxA8 and HoxB10), with no direct mouse such as deep mixing, iron deficiency and in genomic clusters and, importantly, they equivalents (Fig. 1). Moreover, the expres- heavy grazing pressure, have been invoked to are expressed in a spatially colinear fashion sion domains of the anterior Hox genes are explain the HNLC condition. An in situ iron — anterior genes are expressed early in partly overlapping, and restricted to a short- fertilization experiment (IronEx II), carried development and towards the front of the er anterior region. Possibly the most impor- out in the South Equatorial Current adjacent body, posterior genes later in development tant finding is that the zebrafish has at least to the EUZ, yielded a spectacular diatom and in more distal portions of the body. two additional Hox gene clusters for a total of bloom4 and showed that iron availability In invertebrates, only a single Hox gene six and not, as previously thought8, the typi- indeed limited new production in this region. cluster has been found (although it is split in cal vertebrate number of four. All of the Dugdale and Wilkerson argue that, as the Drosophila). The common ancestor of all genes on these additional clusters have prob- EUZ diatoms are already silicate-limited, chordates is surmised to have had a single ably not yet been discovered, and three are adding iron should have no effect on them. cluster as well. This cluster is thought to reported so far1. They suggest that iron upwelling with the have duplicated to four clusters (A–D) on These two additional clusters lead us to other nutrients in the EUZ is sufficient to different chromosomes, accompanying the question a simple, ‘more clusters, more com- meet the demands of the diatoms. In the increasing complexity of body plans during plexity’ model of evolutionary diversifica- iron-limited waters of the South Equatorial the evolution of vertebrates (Fig. 1). But a tion — in terms of phenotypic complexity, Current, iron-fertilized diatom growth report by Prince et al.1, shortly to appear however measured, a zebrafish is probably would eventually be halted by silicate but in Development, is likely to cause some not 50 per cent more complex than a mouse NATURE | VOL 391 | 15 JANUARY 1998 225 Nature © Macmillan Publishers Ltd 1998 news and views Zebrafish (42) Pufferfish (31) Mouse (39) 13 12 11 10 9 8 7 6 5 4 3 2 1 13 12 11 10 9 8 7 6 5 4 3 2 1 13 12 11 10 9 8 7 6 5 4 3 2 1 A A A B B B C C C D D D X Y 100 YEARS AGO Loss of 1 Hox gene Loss of 12 Hox genes Loss of 5 Hox genes Messrs. Swan Sonnenschein and Co. Cluster duplications announce that they will shortly publish a 13 12 11 10 9 8 7 6 5 4 3 2 1 work, entitled “The Wonderful Century: its8 Hypothetical A Successes and its Failures,” by Dr. Alfred fish ancestral B (43) condition C R. Wallace, F.R.S. The object of the D Lost Hox gene volume is to give a short descriptive Loss of 1 Hox gene Hox pseudogene sketch of all the more important mechanical inventions and scientific 13 12 11 10 9 8 7 6 5 4 3 2 1 discoveries which are distinctive of the Hypothetical A B (44) nineteenth century. ... The author vertebrate ancestral C condition D maintains that our century is altogether unique; that it differs from the eighteenth Loss of 8 Hox genes or seventeenth centuries, not merely as those differed from the centuries which 13 12 11 10 9 8 7 6 5 4 3 2 1 A immediately preceded them, but that it B (52) C has initiated a new era, and that it may D be more properly compared with the whole preceding historical period. Cluster duplications 13 12 11 10 9 8 7 6 5 4 3 2 1 The January number of the National Hypothetical chordate Review has an admirable article by Mr.
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