Friday, 24 October 2014

Butterfly tennis balls!

A new study published in the journal PLOS Genetics (23 October 2014, PLOS Genet 10(10): e1004698) shows some very striking images of developing butterfly embryos; they look like little tennis balls! Dr Melanie Gibbs of the Centre for Ecology & Hydrology (CEH), one of the authors on the paper, explains where this unusual pattern comes from and how it may be linked to offspring survival.

Butterfly tennis balls: ShxA expression in 10 hour old embryos.
Photo by Jean-Michel Carter

“One of the first things that happens when insects begin to develop inside a freshly laid egg is that cells differentiate into those that will become the embryo, and those that will form extraembryonic tissue. The extraembryonic tissue covers the embryo and consists of a number of membranes, most notably the amnion and the serosa.

Hox genes are normally involved in patterning the embryo from head to tail, but one Hox gene called zerkn├╝llt (zen) took on a new role and became involved in extraembryonic tissue formation in insects.

A collaborative project led by researchers at University of Oxford working with scientists at Oxford Brookes University and CEH has recently found that during the evolution of butterflies and moths, zen duplicated a number of times resulting in four novel genes, called the Special homeobox genes (shx). Although zen has been shown to duplicate in other insect orders, such a large number of zen-derived genes has never been witnessed before. This begs the question; what do they do?

During his PhD, Jean-Michel Carter (co-supervised by Dr. Casper Breuker, Oxford Brookes University and myself at CEH) found that in the Speckled Wood butterfly (Pararge aegeria) mothers put RNA transcripts of two of these genes, ShxC and ShxD, into the eggs they produce in their ovaries. These transcripts are put in the eggs in the location where the extraembryonic tissue will form. Such localisation actually represents one of the most complex examples of RNA localisation within a cell ever reported in any species, with the mother outlining the region that will become the future extraembryonic tissue before fertilisation and egg laying has even occurred!

ShxC expression in the egg developing inside the mother’s ovary.
Photo by Jean-Michel Carter

It is possible to visualise the location of specific RNA transcripts by using custom-made probes, called riboprobes, which colour purple when the RNA of interest is detected and bound. When you use such probes for Shx gene transcripts in both the ovaries and developing embryos (at around 10 hours old) and look under the microscope, you see an amazing pattern which closely resembles the pattern on a tennis ball. These patterns become even clearer when the embryo itself also starts expressing the ShxA and ShxB genes in the extraembryonic region which will become the serosa. So we started wondering what is a serosa exactly, and is it important? We are also intrigued as to why Speckled Wood mothers go to such lengths to make sure that this tissue is specified even before fertilisation occurs.

The insect serosa is considered to be an evolutionary novelty, which has been linked with the successful colonisation of the land by a large number of insect orders. For example, their predominantly aquatic sister group, the crustaceans, do not have a serosa. Apart from protecting the embryo from drying out, the serosa may also play a role in the innate immune system and the processing of environmental toxins. Thus by ensuring that the serosa develops correctly, butterfly mothers can therefore greatly improve their offspring’s chances of developing successfully and surviving to hatch from the egg, in often hostile and changeable terrestrial environments.”

Melanie Gibbs

A Speckled Wood female laying an egg.
Photo by Casper Breuker

Additional information

Full paper reference: Ferguson L, Marletaz F, Carter J-M, Taylor WR, Gibbs M, Breuker CJ & Holland PWH. 2014. Ancient expansion of the Hox cluster in Lepidoptera generated four homeobox genes implicated in extra-embryonic tissue formation, PLOS Genetics 10 (10): e1004698; doi: 10.1371/journal.pgen.1004698

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