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In Press

Brena, C. and M. Akam, The embryonic development of the centipede Strigamia maritima. Developmental Biology, in press.

Pavlopoulos, A. and Akam, M. (2011). The Hox gene Ultrabithorax subtly regulates distinct sets of target genes at successive stages of haltere morphogenesis and differentiation. Proc. Natl. Acad. Sci. USA


Steinmetz, P. R. H., Urbach, R., Posnien, N., Eriksson, J., Kostyuchenko, R. P., Brena, C., Guy, K., Akam, M., Bucher, G. and Arendt, D. (2010)  Six3 demarcates the anterior-most developing brain region in bilaterian animals.   Evo-Devo 1, 14.

Eriksson, J., Tait, N. N., Budd, G. E., Janssen, R. and Akam, M. (2010) Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev. Genes Evol. 22, 117-122

Garcia-Solache, M., Jaeger, J. and Akam, M. (2010) A systematic analysis of the gap gene system in the moth midge Clogmia albipunctata. Dev. Biol. 344, 306-318

Janssen, R., Eriksson, B.J., Budd, G., Akam, M., and Prpic, N. (2010)  Gene expression patterns in an onychophoran reveal that regionalisation predates limb segmentation in pan-arthropods. Evolution and Development 12, 363-372.

Vedel, V., Apostolou, Z., Arthur, W., Akam, M. and Brena, C. (2010)  An early temperature sensitive period for the variation in segment number in the centipede Strigamia maritima. Evolution and Development 12, 347-352.

Reed, H.C., Hoare, T., Thomsen, S., Weaver, S., Akam, M. and Alonso, C. (2010) Alternative splicing modulates Ubx protein function in Drosophila melanogaster. Genetics 184, 745-758.

Jostins, L. and Jaeger, J. (2010) Reverse engineering a gene network using a parallel asynchronous evolutionary strategy. BMC Systems Biology, 2010. 4, 17


Ashyraliyev, M., Siggens, K., Janssens, H., Blom, J., Akam, M. and Jaeger, J., (2009) Gene circuit analysis of the terminal gap gene huckebein. PLOS Comp. Biol. 5, e1000548

Pavlopoulos, A., Kontarakis, Z., Liubicich, D. M., Serano, J. M., Akam, M., Patel, N. H. and Averof, M. (2009) Probing the evolution of appendage specialisation by Hox gene  misexpression in an emerging model crustacean. Proc. Natl. Acad. Sci. USA 106, 13897-13902.

Eriksson, B. J., Tait, N. N., Budd, G. E., and Akam, M. (2009) The  involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid 1996). Dev. Genes Evol. 219, 249-264.

Vedel, V., Brena, C. and Arthur, W. (2009) Demonstration of a heritable component of the variation in segment number in the centipede Strigamia maritima. Evol. Dev. 11, 434-440.
Jaeger, J.  Modelling the Drosophila embryo. Molecular Biosystems 2009, 1549-1568.

Liubicich, D. M., Serano, J. M., Pavlopoulos, A., Kontarakis, Z., Protas, M. E., Kwan, E., Chatterjee, S., Tran, K. D., Averof, M. and Patel, N. H. (2009). Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. Proc. Natl. Acad. Sci. USA 106, 13892-13896.

Panfilio, K. A. (2009). Late extraembryonic morphogenesis and its zenRNAi-induced failure in the milkweed bug Oncopeltus fasciatus. Dev. Biol. 333, 297-311.



Vedel, V., Chipman, A. D., Akam, M. and Arthur, W. (2008) Temperature dependent plasticity of segment number in an arthropod species: the centipede Strigamia maritima. Evolution and Development 104, 487-492.

Chipman, A. D. and Akam, M. (2008) The segmentation cascade in the centipede Strigamia maritima:   Involvement of the Notch pathway and pair-rule gene homologues. Dev. Biol. 319, 160-169.

Dacks, J. B., Walker, G. and Field, M. (2008) Implications of the new eukaryotic systematics for parasitologists. Parasitology International  57, 97-104.

Darlington, J. P. E. C., Benson, R. B., Cook, C. E. and Walker, G. (2008) Resolving relationships in some African fungus-growing termites (Termitidae, Macrotermitinae) using molecular phylogeny, morphology, and field parameters. Insectes Sociaux 55, 256-265.

Jaeger, J., Irons, D. and Monk, N. (2008) Regulative feedback in pattern formation:  towards a general relativistic theory of pattern formation. Development 135, 3175-3183.

Kulakova, M., Cook, C. E. and Andreeva, T. F. (2008) Parahox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa). BMC Developmental Biology  8, 61.

Panfilio, K. (2008) Extraembryonic development in insects and the acrobatics of blastokinesis. Dev. Biol. 313, 471-491.

Peel, A.D. (2008) The evolution of developmental gene networks. Phil. Trans. Roy. Soc. Lond. B. Biol. Sci. 363, 1539-1547.


Pavlopoulos, A. and Akam, M. (2007) Hox go omics:  Insights from Drosophila on Hox gene function. Genome Biology  8, 208.

Peel, A. and Akam, M. (2007) The dynamics of yolk deposition in the grasshopper Schistocerca gregaria. J. Insect Physiol. 53, 436-443.

Panfilio, K. and Akam, M. (2007) A comparison of Hox3 and Zen protein coding sequences in taxa that span the Hox3/ zen divergence. Dev. Genes. Evol. 217, 323-349.

Kulakova, M., Bakalenko, N., Novikova, E., Cook, C. E., Eliseeva, E., Steinmetz, P., Kostyuchenko, R. P., Dondua, A., Arendt, D., Akam, M. and Andreeva, T.  (2007) Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa. Dev. Genes. Evol.. 217, 39-54.


Brena, C., Chipman, A. D., Minelli, A. and Akam, M. (2006) The expression of trunk Hox genes in the centipede Strigamia maritima: Sense and antisense transcripts. Evol. Dev. 8, 252-265.

Peel, A. D., Telford, M.J. and Akam, M. (2006) The evolution of hexapod engrailed-family genes:  Evidence for conservation and concerted evolution. Proc. Roy. Soc. Lond. B 273, 1733-1742.

Panfilio, K., Liu, P., Akam, M. and Kaufmann, T. (2006) Oncopeltus fasciatus zen is essential for serosal tissue function in katatrepsis. Dev. Biol. 292, 226-243.

Chipman, A. D. and Stollewerk, A. (2006). Specification of neural precursor identity in the geophilomorph centipede Strigamia maritima. Dev. Biol. 290, 337-350.

Jaeger, J. and Reinitz, J. (2006). On the dynamic nature of positional information. BioEssays 28, 1102-1111.

Stollewerk, A. and Chipman, A. D. (2006). Neurogenesis in myriapods and chelicerates and its importance for understanding arthropod relationships. Integrative and Comparative Biology 46, 195-206.


Peel, A. D., Chipman, A. D. and Akam, M. (2005). Arthropod segmentation:  Beyond the Drosophila paradigm. Nature Rev. Genet. 6, 905-916.

Negre, B., Casillas, S., Suzanne, M., Sanchez-Herrero, E., Akam, M., Nefedov, M., Barbadilla, A., de Jong, P. and Ruiz, A. (2005) Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox complex. Genome Research 15, 692-700

Cook, C.E., Q.-Y. Yue and Akam, M. (2005) Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic. Proc. Roy Soc. 272, 1295-1304.

Mirth, C. K. (2005). Ecdysteroid control of metamorphosis in the differentiating adult leg structures of Drosophila melanogaster. Dev. Biol. 278, 163-174.

Extavour, C. G. (2005). The fate of blastomeres with respect to germ cell formation in the amphipod crustacean Parhyale hawaiensis. Dev. Biol. 277, 387-402.

Extavour, C., Pang, K., Matus, D. Q. & Martindale, M. Q.  (2005) vasa and nanos expression patterns in a sea anemone and the evolution of bilaterian germ cell specification mechanisms Evolution and Development 7, 201-215

Cook, C. E. (2005). The complete mitochodrial genome of the stomatopod crustacean Squilla mantis. BMC Genomics 6:105

Arthur, W. and Chipman, A. D. (2005) How does arthropod segment number evolve?  Some clues from centipedes. Evol. Dev. 7, 600-607.

Arthur, W. and Chipman, A. D. (2005). The centipede Strigamia maritima:  What it can tell us about the development and evolution of segmentation. BioEssays 27, 653-660


Chipman, A. D., Arthur, W. and Akam, M. (2004) A double segment periodicity underlies segment generation in centipede development. Current Biology 14, 1250-1255.

Cook, C. E., Jiménez, E., Akam, M. and Saló, E. (2004) The Hox gene complement of acoel flatworms, a basal bilaterian clade. Evol. Dev. 6:154-163.

Chipman, A. D., Arthur, W. and Akam, M. (2004) Early Development and Segment Formation in the Centipede Strigamia maritima (Geophilomorpha). Evol. Dev. 6, 78-89

Extavour, C. G. (2004) Hold the germ cells, I'm on duty. BioEssays 26, 1263-1267.

Peel, A. (2004) The evolution of arthropod segmentation mechanisms. BioEssays 26, 1108-1116.

Telford, M. J. (2004) The multimeric b-thymosin found in nematodes and arthropods is not a synapomorphy of the Ecdysozoa. Evol. Dev. 6, 90-94.

Littlewood, D. T. L., Telford, M.J. and Bray, R. A. (2004). Protostomes and Platyhelminthes: the worm's turn. In Assembling the Tree of Life,  (ed. M. Donoghue and C. J.). New York: Oxford University Press.


Extavour, C. G. and Akam, M. (2003) Mechanisms of metazoan germ cell specification: epigenesis and preformation. Development 130, 5869-5884.

Peel, A. and Akam, M. (2003) Evolution of segmentation: Rolling back the clock. Current Biology 13, R708-R710

Alonso, C.R. and Akam, M. (2003)  A Hox gene mutation that triggers Nonsense-mediated RNA Decay and affects alternative splicing during Drosophila development. Nucleic Acids Research 203, 3873-3880.

Roch, F., Alonso, C. and Akam, M. (2003) Drosophila miniature and dusky encode ZP proteins required for cytoskeletal reorganisation during wing morphogenesis. J. Cell Science 116, 1199-1207.

Bourlat, S. J., Nielsen, C., Lockyer, A. E., Littlewood, D. T. J. and Telford, M. J. (2003)  Xenoturbella is a deuterostome that eats molluscs. Nature 424, 925-928.

Stern, D. L. (2003) The Hox gene Ultrabithorax modulates the shape and size of the third leg of Drosophila by influencing diverse mechanisms. Developmental Biology 256, 355-366.

Telford, M. J. and Budd, G. E. (2003) The Place of Phylogeny and Cladistics in Evo/Devo research. Int. J. Dev. Biol. 47, 479-490.

Telford, M. J., Lockyer, A. E., Littlewood, D. T. L. and Cartwright-Finch, C. (2003) Acoelomorphs are the most basal bilaterian phylum and are unrelated to other flatworms. Proc. Roy. Soc. Lond. B 270, 1077-1083.


Chang, C.-C., Dearden, P. and Akam, M. (2002)  Germ line development in the Locust Schistocerca gregariavasa as a marker. Dev. Biol. 252: 100-118.

Rozowski, M. and Akam, M. (2002)  Hox gene control of segment specific bristle patterns in Drosophila. Genes and Development 16, 1150-1162.

Mirth, C. and Akam, M. (2002)  Joint Development in the Drosophila Leg: Cell Movements and Cell Populations. Developmental Biology 246, 391-406

Alonso, C. (2002). Hox proteins: Sculpting body parts by activating localised cell death. Current Biology 12, R776-R778.

Chang, C.-C. and Cook, C. E. (2002) Trends in genomic 'evo-devo'. Genome Biology 3, 4019

Cook, C. and Mostovski, M. (2002). 16S mitochondrial sequences associate morphologically dissimilar males and females of the family Phoridae (Diptera). Biol. J. Linn. Soc. 77, 267-273.

Rozowski, M. (2002)  Establishing character correspondence for sensory organ traits in flies: Sensory organ development provides insight for reconstructing character evolution. Mol. Phylog. Evol. 24, 400-411.

Telford, M. J. (2002) Cladistic analyses of molecular characters: The good the bad and the ugly. Contr. Zool. 71, 93-100.


Alonso, C., Maxton-Kuechenmeister, J. and Akam, M. (2001)  Evolution of Ftz protein function in insects. Current Biology 11, 1473-1478.

Dearden, P.K. and Akam, M. (2001)  Early embryo patterning in the grasshopper, Schistocerca gregaria:  wg, dpp and caudal expression. Development 128, 3435-3444.

Cook, C., Smith, M.L., Telford, M., Bastianello, A. and Akam, M. (2001)  Hox genes and the phylogeny of the arthropods. Current Biology 11, 759-763.

Andreeva, T.F., Cook, C.E., Korchagina, N.M., Akam, M. and Dondua, A.K. (2001) Cloning and analysis of structural organisation of Hox genes in the polychaete Nereis virens  (in Russian). Ontogenesis 32, 225-233.


Dearden, P. and Akam, M. (2000) Segmentation in silico. Nature 402, 131-132.

Dearden, P., Grbic, M., Falciani, F. and Akam, M. (2000). Maternal expression and early zygotic regulation of the Hox3/zen gene in the grasshopper Schistocerca gregaria. Evol. Dev. 2, 261-270.

Akam, M. (2000). Arthropods: Developmental diversity within a (super) phylum. Proc. Natl. Acad. Sci. USA 97, 4438-4441.

Dearden, P. and Akam, M. (2000)  A role for fringe in segment morphogenesis but not segment formation in the grasshopper Schistocerca gregaria. Dev. Genes Evol. 210, 329-336.

Roch, F. and Akam, M. (2000)  Ultrabithorax and the control of cell morphology in Drosophila halteres. Development 127, 97-107.


How to turn a wing into a haltere - Hox gene targets during metamorphosis

Hox genes are the master regulators that cause different parts of the body to develop into different structures – for example, into mouthparts on the head, but legs on the thorax. It is still not known how Hox genes bring about these complex changes.  In work published recently in the Proceedings of the National Academy of Sciences (USA), we have shown that the set of downstream targets regulated by one Hox gene changes dramatically as development proceeds.

We have studied the Hox gene Ultrabithorax, (Ubx for short) in fruit flies. In all insects, Ubx is active in the hind wings to make them different from the forewings. In flies, this difference is dramatic – the hind wings develop as small round balancing organs called halteres, while the forewings forms the large flat wing blades used for flying.   We have engineered a system that allows us to activate the Ubx gene in developing wing blades, where it would not normally be expressed. If activated throughout development, this causes the wing blades to develop as reduced balloon-like structures resembling halteres, (see picture above).  However, we can also turn Ubx on at precisely controlled times during development, and then measure its effects in the wing with assays that monitor the activity of thousands of other genes in the genome (microarray profiling and quantitative RT-PCR).

We find that the spectrum of genes regulated by Ubx changes dramatically as the animal proceeds through metamorphosis, from larva to pupa to developing adult.  This explains, at least in part, how just one gene can orchestrate such complex changes in the shape and size of an organ.

The Hox gene Ultrabithorax regulates distinct sets of target genes at successive stages of Drosophila haltere morphogenesis, PNAS USA, 108(7): 2855-2860].