Evolutionary origins and molecular mechanisms of hostplant adaption in lepidopteran herbivores [Elektronische Ressource] / von Hanna Marieke Heidel-Fischer

Hfischer

Informations

• Publié par: friedrich-schiller-universitat_jena
• Publié le: 01 janvier 2009
• Nombre de lectures: 16
• Langue: English

Extrait

Evolutionary Origins and Molecular Mechanisms of
Hostplant Adaptation in Lepidopteran Herbivores



Dissertation
zur Erlangung des akademischen Grades
doctor rerum naturalium (Dr. rer. nat.)


Vorgelegt dem Rat der Biologisch-Pharmazeutischen Fakultät
der Friedrich-Schiller-Universität Jena




von Diplom-Biologin
Hanna Marieke Heidel-Fischer

geboren am 14. Juli 1977 in Berlin































Contents
Contents

1. General introduction...............................................................................................................5
2. Chapter I: Evolutionary origins of a novel hostplant detoxification gene in butterflies ......14
2.1 Introduction.....................................................................................................................15
2.2 Material and Methods .....................................................................................................17
2.3 Results.............................................................................................................................22
2.4 Discussion.......................................................................................................................31
3. Chapter II: Microevolutionary dynamics of a macroevolutionary key innovation in a
Lepidopteran herbivore.............................................................................................................40
3.1 Introduction.....................................................................................................................41
3.2 Material and Methods44
3.3 Results.........46
3.4 Discussion.......................................................................................................................52
4. Chapter III: Gene expression in a generalist butterfly upon feeding on different hostplants
..................................................................................................................................................59
4.1 Introduction......60
4.2 Material and Methods .....................................................................................................62
4.3 Discussion......70
5. General discussion................................................................................................................76
6. Summary...............................................................................................................................85
7. Zusammenfassung ................................................................................................................87
8. Acknowledgements ..............................................................................................................90
9. References ............................................................................................................................91
10. Selbständigkeitserklärung...................................................................................................99
11. Curriculum Vitae ..............................................................................................................100
12. Publications ......................................................................................................................101




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4 General introduction
1. General introduction

The intimate interactions between herbivorous insects and their food plants have resulted in
their coevolution wherein phytophagous insects overcome plant defenses followed by plants
counter-adapting to herbivorous insect feeding damage. This constant arms race between
plants and insect herbivores was first postulated by Ehrlich and Raven in 1964 and is one of
the foundations of insect-plant interactions research. Although the ecology of this co-
evolutionary arms race is mostly well understood, an understanding of the molecular
mechanisms is still lacking. In particular, molecular insight remains scarce on the insect side
of this interaction with little known about the mechanisms used by insects to adapt and
metabolize plant allelochemicals. Thus, developing a molecular understanding of insect
coevolutionary innovations is very important to understanding the evolution of plant-insect
interactions and adaptive processes in general.

Molecular mechanisms for adaptive mutations
As most plants have evolved chemical antiherbivory defenses, successful feeding on plants
requires an efficient detoxifying mechanism. Adaptive mutations allowing an insect to utilize
a new food plant can have different molecular origins, affecting the regulatory regions as well
as the coding sequence of genes. Mutations in the cis-regulatory regions can either alter the
expression level of genes or it can result in expression in different tissues or developmental
stages. As a consequence, the organismal phenotype can be dramatically affected. Schlenke
and Begun (2004) showed that an insertion of a transposable element in the cis-regulatory
region of Cyp6g1 is associated with increased expression in a Drosophila simulans
population. Cyp6g1 has been shown to be responsible for DDT resistance in Drosophila
melanogaster (Daborn et al. 2002). Surveys of D. simulans populations show that lineages
with the transposable insertion exhibit evidence of strong directional selection suggesting
selection for resistance to an insecticide, a natural toxin or an environmental contaminant
(Schlenke and Begun 2004). In Anopheles gambiae the expression of one quarter of the
detoxification genes is developmentally regulated, indicating the importance of cis-regulation
for the specificity of detoxification genes in this species (Strode et al. 2006).

Point mutations, insertions or deletions within the coding region can result in novel gene
function, allowing for rapid adaptation to new environments. In D. melanogaster the insertion
5 General introduction
of a transposable element within the coding region of a gene resulted in a truncated gene
product that nevertheless generated a functioning protein. The truncated protein appears to
increase resistance to an organophosphate pesticide and population surveys indicate that this
novel gene product has spread across D. melanogaster populations (Aminetzach, Macpherson,
and Petrov 2005). Li et al (Li, Schuler, and Berenbaum 2003) provided evidence of how shifts
in host plant utilization in two Papilio species were associated with the evolution of the
corresponding P450 sequence which facilitated hostplant specialization.

Gene duplications also play a very important role in the evolution of detoxification
mechanisms, either by tandem or relocation duplication of a gene fragment, a whole gene, or
a whole chromosomal fragment (Force et al. 1999; Lynch 2007). Although genomic resources
suggest that duplication events arise at a very high rate of about 0.01 per gene per million
years (Lynch and Conery 2000), the most common fate of duplicated genes will be silencing
and loss. Only a small amount of duplicates are retained as functional genes. Such paralogous
genes could facilitate adaptive evolution in two ways. Either one paralog could acquire a new
function (neofunctionalization), or both duplicates could divide the existent function of the
gene (subfunctionalization). In Papilio polyxenes for example, a duplicated P450 gene
underwent subfunctionalization resulting in two paralogous genes, CYP6B1 and CYP6B3
which show different efficiencies in metabolizing plant allelochemicals (Wen et al. 2006).
Such gene duplication events, followed by neofunctionalization or subfunctionalization, are
likely to be the origin of many detoxifying enzymes in insects.

Phase I and phase II detoxifaication
Metabolism and thereby detoxification of lipophilic toxins into more hydrophilic products
typically occurs in two phases. In phase I, a primary product is formed, that might in some
cases be more toxic than the parent molecule but in other cases might already be ready for
excretion. In the phase II, the primary products are metabolized into secondary products that
can be directly excreted (Brattsten 1992). This type I and II categorization is primarily applied
to the metabolization of drugs in animals and humans and also provides a useful perspective
for considering the metabolism of plant allelochemicals in phytophagous insects.

Although to date knowledge is scarce about the mechanisms applied by insect to metabolize
plant allelochemicals, in general it is assumed that phase I and phase II detoxifying enzymes
play a major role detoxifying plant compounds in insects. Many studies have found the phase
6 General introduction
I enzyme cytochrome P450 monooxygenase to be important across lepidopteran and other
insects in the detoxification of plant allelochemicals and other toxins (Pet