I am generally interested in the molecular and cellular mechanisms of the emergence of pattern and form during animal development, and in particular how these mechanisms change in the course of evolution.  

The insects are an ideal model clade with which to approach these questions, due to their species richness, developmental diversity, and the ability to test gene function in a number of species representing a broad phylogenetic range.  

Currently two major topics are the foci of my work:  1) The evolution of mechanisms for establishing and patterning the dorsal-ventral (DV) axis of insect embryos, and 2)  The evolution of germline establishment and function in insects, primarily focusing on holometabolous insects.  In both cases the wasp Nasonia vitripennis is the main model employed to gain insights into the evolution of these processes.  This species has the advantages that it is easily kept in the lab, has a fully sequenced genome, and is amenable to both parental RNAi and germline transformation to test gene function (conditions for the latter are currently being optimized).

Evolution of DV patterning mechanisms
 

I. Maternal specification of DV polarity

 In Drosophilapatterning of the DV axis begins with the migration of the oocyte nucleus to the anterior pole where it remains attached to the cortex in a position that is asymmetric with respect to the short axis of the egg chamber.  mRNA for gurken localized around the oocyte nucleus is translated and activates EGF signaling in the overlying somatic follicle cells, which induces DV asymmetry in these cells which is passed back to the embryo after egg laying.  My previous work has shown that  germline to soma signaling mediated by EGF is a conserved feature of insect oogenesis and embryonic DV patterning (Lynch et al., Current Biology, 2010).  However, it was also found that the mechanisms by which DV patterning information is transmitted from the follicle cells to the later embryo must be different.  The nature of this signal, as well as how the generation and elaboration of the initial DV asymmetry change in the course of evolution in response to selective pressure on oogenesis and early embryogenesis, are current topics of interest.
 

At left, a Tribolium egg chamber, with f-actin labeled in green, and activated MAPK in red. At right, a Nasonia egg chamber, DNA labeled in blue, tgf-alfa (gurken) mRNA labeled in red.

II. DV patterning in the embryo

  In Drosophila, two signaling pathways are largely responsible for setting gene expression domains that give rise to different cell fates along the DV axis: Toll/Dorsal signaling on the ventral side, and Dpp/BMP signaling on the dorsal side.   Toll signaling plays the primary role in the Drosophila embryo, with many Dpp signaling components downstream of the Dorsal gradient.  We are taking advantage of the very similar, independently derived, mode of long germ embryogenesis of Nasonia as a model to understand the variety of strategies available to and the constraints restricting evolution in the derivation of long germ embryogenesis.  Preliminary results obtained by two graduate students, Thomas Buchta and Orhan Özüak, indicate that DV patterning is much more dynamic in Nasonia compared to Drosophila, and that the relative inputs of Toll and BMP signaling in patterning the axis are quite divergent in the wasp.  We intend to take advantage of the genomic and functional resources available in Nasonia to characterize the regulatory network underlying DV patterning in the wasp in enough detail to make meaningful comparisons to Triboliumand Drosophila, which should allow inferences as to how this network has been altered over the course of phylogeny, and in the process of transitions to long germ patterning.

At left, Tribolium embryo stained for cactus (red) and short-gastrulation (green). Right, a Nasonia embryo stained for twist (red), vnd (green), and DNA (blue).

III.Evolution of germline determination mechanisms in holometabolous insects

In Drosophilaa specialized cytoplasm localized to the posterior pole of the oocyte and embryo, termed “pole plasm” , is necessary and sufficient for the induction of the primordial germ cells (pole cells) early in embryogenesis.  The regulatory network required for the production, behavior, and maintenance of this cytoplasm includes proteins that are highly conserved among all animals (e.g., Vasa, Piwi, Staufen, Nanos) and apparently novel genes (e.g., Oskar, Polar Granule Component).  The use of maternally generated pole plasm and pole cells for germline determination appears to be restricted to holometabolous insects, and is found in species representing the major lineages of this clade (e.g. Nasonia (Hymenoptera (ants, bees, and wasps)), Acanthoscelides, Callosobruchus (Coleoptera (beetles)), Pectinophora(Lepidoptera (butterflies and moths)), and most Diptera (flies).  However, these mechanisms are missing in several species, including the honeybee Apis, the beetle Tribolium, and the silkmoth Bombyx, indicating the strategies for germline determination are evolutionarily quite labile.   We are using Nasonia, which produces a form of posterior pole plasm (called the “oosome”) and pole cells to gain a picture of the ancestral constitution of maternal germ plasm regulatory networks among the Holometabola, and have found that many of the players have highly conserved roles, with some lineage specific differences. These analyses will be extended to gain a more complete understanding of the regulatory network responsible for the formation of the oosome, which will allow a robust comparison to the network employed in Drosophila.   We are also interested in understanding how the germline is determined in species, such as Tribolium, that have secondarily lost the ability to assemble maternal pole plasm.

Nasonia embryos of progressively older ages, stained for otd1 (green), nanos (red), and DNA (blue)

Join us in Cologne for the 2012 International Nasonia Genome meeting. (Details coming soon….)

Contact information:

DSc. Jeremy Lynch

Institut of Developmental Biologie

Zuelpicher Str. 47B

50674 Cologne

Germany

Email: jlynch[at]uni-koeln.de

Phone: +49-221-470-2618

Curriculum vitae (pdf 144kb)

Links:

About Nasonia:

NasoniaBase:

Publications:

Lynch, J., Desplan, C. Evolution of development: beyond bicoid. Current Biology. 2003 Jul 15;13(14):R557-9. doi:10.1016/S0960-9822(03)00472-X 

Lynch, J., Desplan, C. ‘De-evolution’ of Drosophila toward a more generic mode of axis patterning. International Journal of Developmental Biology. 2003. Evolution of Development special issue.

Shuker D, Lynch J, Peire-Morais A. Moving from model to non-model organisms? Lessons from Nasonia wasps. Bioessays. 2003 Dec;25(12):1247-8. doi: 10.1002/bies.10367

Pultz MA, Westendorf L, Gale SD, Hawkins K, Lynch J, Pitt JN, Reeves NL, Yao JC, Small S, Desplan C, Leaf DS. A major role for zygotic hunchback in patterning the Nasonia embryo. Development. 2005 Aug;132(16):3705-15. doi: 10.1242/dev.01939

Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C. Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature. 2006 Feb 9;439(7077):728-32. doi:10.1038/nature04445 Featured in Faculty of 1000

Lynch JA, Olesnicky EC, Desplan C. Regulation and function of tailless in the long germ wasp Nasonia vitripennis. Development Genes and Evolution. 2006 Jul;216(7-8):493-8. doi: 10.1007/s00427-006-0076-5

Lynch JA and Desplan, C. A method for parental RNA interference in the wasp Nasonia vitripennis. Nature Protocols 1, 486 - 494 (2006). doi:10.1038/nprot.2006.70

Tribolium genome sequencing consortium (Member). The genome of the model beetle and pest Tribolium castaneum. Nature. 2008 Apr 24;452(7190):949-55. doi:10.1038/nature06784

Rosenberg MI, Lynch JA, Desplan C. Heads and tails: evolution of antero-posterior patterning in insects. Biochim Biophys Acta. 2009 Apr;1789(4):333-42. doi:10.1016/j.bbagrm.2008.09.007

Fonseca RN, Lynch JA, Roth S. Evolution of axis formation: mRNA localization, regulatory circuits and posterior specification in non-model arthropods.Current Opinions in Genetics and Development. 2009 Aug;19(4):404-11. doi:10.1016/j.gde.2009.04.009

Roth S, Lynch JA. Symmetry breaking during Drosophila oogenesis. Cold Spring Harbor Perspectives in Biology. 2009 Aug;1(2): a001891.

Nasonia Genome Working Group, Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, Beukeboom LW, Desplan C, Elsik CG, Grimmelikhuijzen CJ, Kitts P, Lynch JA, et al., Functional and evolutionary insights from the genomes of three parasitoid Nasonia species.Science. 2010 Jan 15;327(5963):343-8. (Founding member of Nasonia Genome Working Group) doi: 10.1126/science.1178028

Lynch JA*, Peel AD, Drechsler A, Averof M, Roth S. EGF Signaling and the Origin of Axial Polarity among the Insects Current Biology. 2010 Jun 8;20(11):1042-7. doi:10.1016/j.cub.2010.04.023

Rousso T, Lynch JA, Yogev S, Roth S, Schejter ED, Shilo BZ. Generation of distinct signaling modes via diversification of the Egfr ligand-processing cassette. Development. 2010 Oct;137(20):3427-37. doi: 10.1242/dev.049858

Lynch JA*, Desplan C. Novel modes of localization and function of nanos in the wasp Nasonia. Development. 2010 Oct 7. [Epub ahead of print] doi: 10.1242/dev.054213

Lynch JA, Roth S. The Evolution of Dorsal-ventral Patterning Mechanisms in Insects. Genes & Development. 2011 25: 107-118. doi:10.1101/gad.2010711

Lynch JA*, Özüak O, Khila A, Abouheif E, Desplan C, Roth S. The Phylogenetic Origin of oskar Coincided with the Origin of Maternally Provisioned Germ Plasm and Pole Cells at the Base of the Holometabola. PLoS Genetics.  20117(4): e1002029. doi:10.1371/journal.pgen.1002029.   (Featured in accompanying article:  Extavour CG (2011) Long-Lost Relative Claims Orphan Gene:oskar in a Wasp. PLoS Genetics 7(4): e1002045. doi:10.1371/journal.pgen.1002045)

* Corresponding author