Molluscs.org: The web page of Angus
Davison
Research overview: population genetics,
evolution and adaptation
Research in the lab is split between two main themes. First, we are interested in the
evolution and maintenance of colour polymorphisms, and more generally,
how they impact on the speciation and adaptive radiation of snails.
This work is mostly being carried out on the charismatic European snail
Cepaea and the endemic
Japanese genus Mandarina. Second, we have initiated a
programme to establish the pond snail Lymnaea
stagnalis as a model for the understanding of the evolution and
development of left-right asymmetry. The ultimate aim is to understand
how chirality is determined at the molecular level, then extrapolate
this to include the means by which variation in sequence, and dominance
relations between alleles, contributes to the evolution of new chiral
morphs. There are also a number of other projects – research on the
conservation genetics of mustelids has been particularly fruitful
because it links in to the Conservation
Genetics course that I teach. Another avenue is to understand
the function of the ‘love’ dart of snails.
A wide range of techniques are used, including the latest DNA
ultra-high throughput sequencing methods, field work, mathematical
models, phylogenetics and bioinformatics. Research therefore crosses
several other sub-disciplines within the School, including
Developmental Biology and Gene Control, Animal Behaviour and Ecology,
and even Parasite Biology. We also benefit with strong links to Dr.
Aziz Aboobaker in Nottingham, and collaborators in Edinburgh (Professor
Mark Blaxter) and Japan (Professor Satoshi Chiba). Research is largely
funded by The Royal Society, the JSPS and the BBSRC.
Although I am always keen to hear from potential students, I am
particularly keen to recruit a student that may wish to develop
transgenic, in vitro injection or RNAi methods for Lymnaea stagnalis, with a view to
further understanding chirality.
Downloads of my publications are available from the publications
sections of this. PhD studentships are advertised on
http://www.findaphd.com/
PhD projects for 2009 start
I am advertising three possible projects this year, all likely
to be funded by the BBSRC Funding and to be awarded on a competitive
basis within the School of Biology.
The first is being most widely circulated and is most likely to be
filled, but please do not be put off from contacting me if you are more
interested in the other two projects. In common to all, applicants
should have, or expect to receive, a good degree in a relevant subject,
and an interest and
enthusiasm for evolution. Students will experience a variety of ‘core’
methods, depending upon interests and aptitude (e.g. molecular lab
techniques, in situ hybridization, micromanipulation, field work,
ultrahigh-throughput DNA sequencing).
In the first instance, prospective students should send a CV and an
indication of general area of interest to
angus.davison@nottingham.ac.uk.
1. Evolution
and development of mirror-image snails.
Sinistral (anticlockwise-coiling) snails make up much less than 10% of
all snail species. Why are sinistral snails so rare and how do they
evolve? Are sinistrals a perfect mirror image of dextrals, or are there
fitness consequences of being sinistral? How is the left-right
asymmetry of the shell inherited, and at the molecular level, what is
the hypothetical F-molecule that ultimately determines asymmetry?
We are establishing the pond snail Lymnaea stagnalis as a comparative
model organism for the understanding of left-right asymmetry. With
BBSRC funding, and in collaboration with Prof
Mark Blaxter (Edinburgh, Solexa/454 sequencing, bioinformatics), we
have just begun a project to characterise the Lymnaea ‘chirality’
locus, with the ultimate aim to understand the evolution and
development of asymmetry at the molecular level. The work has been
given added impetus because it has recently been discovered that a
common gene links vertebrate and molluscan asymmetry. As the lab is
also investigating molluscan asymmetry from behavioural, evolutionary
and population genetic perspectives, there is a wide scope for PhD
project in any of these areas.
Further reading:
Davison, A et al (2008) Mating behaviour in Lymnaea stagnalis pond snails is a
maternally inherited, lateralised trait. Biology Letters, in press.
Featured in Nature 20 November 2008, p285
Schilthuizen, et al (2008) Sexual selection maintains whole-body chiral
dimorphism in snails. Journal of Evolutionary Biology
20: 1941–1949.
Davison A et al (2005) Speciation and gene flow between snails of
opposite chirality. PLoS Biology 3: e282.
Shibazaki Y, Shimizu M, Kuroda R (2004) Body handedness is directed by
genetically determined cytoskeletal dynamics in the early embryo. Current
Biology 14, 1462-1467.
Schilthuizen M, Davison A (2005) The convoluted evolution of snail
chirality. Naturwissenschaften 92, 504-515.
Asami T, Cowie RH, Ohbayashi K (1998) Evolution of mirror images by
sexually asymmetric mating behavior in hermaphroditic snails. American Naturalist 152,
225-236.
2. Evolution of snail 'love' darts.
Male traits that confer harm on the female may have a direct or
indirect increase in fitness, usually via increased paternity. By far
the best characterised system for the study of the molecular
interactions is Drosophila.
The unfortunate problem is that crucial data from outside the Insecta
are almost entirely lacking. The objective of this project will be to
initiate an analysis of the products contained on the ‘love’ dart of
snails, with a long term view to develop an alternative system for the
understanding of sexual conflict at the molecular level. The project is
in collaboration with Dr. Joris Koene,
Vrije University, Amsterdam, with the lab also benefiting from an
ongoing collaboration with Prof Mark
Blaxter in Edinburgh (sequencing, bioinformatics).
Further reading:
Preece,
T, Mao, Y, Garrahan, JP and Davison,
A (2009) Harmful
mating tactics in hermaphrodites. American
Naturalist, in press.
Davison, A,
Wade, CM, Mordan, PB and
Chiba, S (2005). Sex and darts in slugs and snails (Mollusca:
Gastropoda: Stylommatophora). Journal
of Zoology (London) 267: 329-338. 
Mating
behaviour database.
Cover photo: 
Reviewed in Trends in Ecology and Evolution
20 (11): 581-584.
3. Evolution of supergenes.
Land snails of the genus Cepaea
are perhaps the pre-eminent model organisms for the study of natural
selection, and its effects on genetic polymorphism. In common with
debates about other organisms, there has been discussion about how the
colour polymorphism of Cepaea evolved
into a supergene, a problem that relates to the much wider issue of how
the genome responds to disruptive or balancing selection. The general
objective of this project is to dissect the individual components of
the supergene, and will be led by the interests of the student.
Unwinding snail chirality
For an organism to become asymmetric, bilateral symmetry must somehow
be broken during development. Although multiple lines of enquiry
remain, a deep-seated theoretical problem has stoked a burning interest
in understanding the symmetry-breaking event – how is one side of an
organism consistently distinguished from the other, given that the side
that is called ‘right’ is essentially arbitrary? In the hypothetical
view of Brown and Wolpert, the solution is provided by a pre-existing
asymmetric molecular reference: an asymmetric gradient is created if an
‘F-molecule’ aligns with anterior-posterior and dorsal-ventral axes, so
transporting an effector molecule towards the left or right. Asymmetry
is thus entirely dependent upon the chirality (and subsequent
alignment) of the F-molecule.
To attempt to validate the hypothesis, attention has focussed on the
mouse, chick and zebrafish. In these model organisms, it has been found
that rotational beating of cilia in the early gastrula creates an
asymmetric extracellular fluid movement. It has therefore been argued
that this is the symmetry-breaking step – the chirality of cilial motor
proteins leads to directional fluid movement, ultimately determining
the molecular and morphological asymmetry.
The unfortunate problem, however, is that a body of research indicates
that the symmetry-breaking event sometimes occurs much earlier and at
the intracellular level, preceding the commencement of ciliary
movement. Together, the results suggest that in invertebrates and at
least some vertebrates, molecular asymmetry is established early in
embryogenesis, with morphological asymmetry only becoming apparent
later. In consequence, the field of left-right patterning is “in
disarray”, because the notion that the rotary movement of cilia
determine asymmetry is an elegant hypothesis that is undermined by
earlier symmetry breaking events, even in some vertebrates. If the
rotational beating of cilia is the symmetry-breaking step in the mouse,
then it is probably the exception.
We are therefore developing the pond snail Lymnaea stagnalis as a lab animal
to help understand the symmetry-breaking step, following years of
neglect. The primary motivation for using Lymnaea is that molluscan asymmetry
is established very early, and is genetically tractable; other
“genome-era” molluscs do not vary in their chirality and so are of no
direct use to this project.
The specific aim of a project that has been funded by the BBSRC is to
utilise the power of ultrahigh-throughput DNA sequencing to directly
clone the gene for chirality in Lymnaea
stagnalis, working on the hypothesis that the maternal
determinant of chirality in snail eggs is a molluscan F-molecule, or at
least a molecule that interacts with it. With false positives excluded
by genetic mapping, we will then attempt to definitively identify the
gene with functional and cytological studies.
The general, long-term aim is put in place techniques that will in the
future enable a precise understanding of the symmetry-breaking event in
snails, stimulating investigative analyses of the same or related
molecules in other organisms, including vertebrates. The work is timely
because very recent technological advances have made identification of
the asymmetry-determining locus feasible within the scale of a three
year grant. Much of the work will be outsourced (e.g. sequencing,
genotyping)
Some further background. The impetus for this project arose directly
from work that I began while I was employed by the Royal Society in
Edinburgh. During the fellowship, one of my research themes was to
understand how sinistral coiling morphs of a land snail evolved, by
comparing molecular phylogenies with morphological data and predictions
based on a mathematical model. The results of the work were published
in PLoS Biology, because the results suggest a general mechanism by
which left-right asymmetry evolves in snails.
Since being employed by Nottingham, I have expanded my studies on snail
chirality. An invited review on the biology of chiral snails stimulated
my thoughts on the molecular mechanisms behind the establishment of
asymmetry (Schilthuizen and Davison 2005), and with others I helped
identify another explanation as to how asymmetry evolves: in some
Malaysian snails, natural selection against new types is probably
counteracted by sexual selection (Schilthuizen et al. 2007).
One problem with prior work on snail chirality has been a lack of
cross-talk between disciplines and model organisms, so I would like to
approach the problem from all angles. The aim now is to take my prior
research on chirality to a logical conclusion, by bringing together a
group of researchers that cover all the relevant disciplines. Having
characterised the snail chirality locus, the ultimate aim is to
understand how chirality is determined at the molecular level, then
extrapolate this to include the means by which variation in sequence,
and dominance relations between alleles, contributes to the evolution
of new chiral morphs.
The work in PLoS Biology was widely reported in the press, including
the popular science blog Pharyngula.
Sex and darts in slugs and snails
In the final stages of an elaborate courtship, many slugs and snails
shoot calcareous ‘love’ darts into each other. While darts improve the
reproductive success of the shooter, by promoting sperm survival in the
recipient, it is unclear why some species have darts and others do not.
In fact, dart use has barely been studied, except in the garden snail Cantareus aspersus (Helix aspersa).
We took an evolutionary approach to attempt to understand the origin
and use of darts (Davison et al 2005), by investigating mating
behaviour in a wide range of species. ‘Face-to-face’ mating behaviour
is restricted to three monophyletic groups of snails and slugs, and
dart-bearing species are a subset within the same groups, which
suggests a link, though not necessarily a causal one. As yet, we are
unable to quantify the extent to which darts or mating behaviour, as
well as several other correlated characters, are determined by common
ancestry or regimes of natural or sexual selection, because our current
phylogeny lacks resolution. However, the results emphasise that to
understand the use of darts, then data are required from a wide range
of species. The realisation that several characters are correlated may
stimulate further research, and could eventually lead to some testable
models for dart and mating behaviour evolution.
This work was featured in a report in the journal Trends in Ecology and
Evolution.