PhD thesis Andreas Kelager

190 Pages·2015·31.14 MB·English

UNIVERSITY OF COPENHAGEN
FACULTY OF SCIENCE
Centre for Social Evolution
Center for Macroecology, Evolution and Climate
PhD thesis
Andreas Kelager
Maculinea alcon
IOTIC INTERACTION IN SPACE AND TIME
B
The social parasitic butter�ly and
its hosts as model system
Academic advisors
Dr. Hans Henrik Bruun and Dr. David R. Nash
Submitted: January 2015

University of Copenhagen
Faculty of Science

B
IOTIC INTERACTION IN SPACE AND TIME
THE SOCIAL PARASITIC BUTTERFLY MACULINEA ALCON AND ITS HOSTS AS MODEL
SYSTEM

Andreas Kelager
PhD thesis | January 2015
Faculty of Science | University of Copenhagen
Author Andreas Kelager

Affiliation Center for Macroecology, Evolution and Climate
Centre for Social Evolution
Department of Biology, University of Copenhagen

Title/subtitle Biotic interaction in space and time: the social parasitic Maculinea
alcon and its hosts as model system.

Academic advisors Dr. Hans Henrik Bruun
Center for Macroecology, Evolution and Climate, University of
Copenhagen
Dr. David Richard Nash
Centre for Social Evolution, University of Copenhagen

Submitted to PhD School of the Faculty of Science,
University of Copenhagen, Denmark
January 2015

Type PhD thesis

Cover The Alcon Blue butterfly, Maculinea alcon (© David Nash), the Marsh
Gentian, Gentiana pneumonanthe (© Bjarne Nielsen), The Ruby Ant,
Myrmica rubra carrying M. alcon larva (© David R. Nash)
Preface

This thesis is product of a three year PhD project on biotic interactions in a changing world
based at the two Center of Exellence, Centre for Social Evolution (CSE) and Center for
Macroecology, Evolution and Climate (CMEC) both funded by the Danish National Research
Foundation. The thesis was supervised by Dr. Hans Henrik Bruun and Dr. David Richard Nash,
but during the PhD period I worked with Dr. Maren Wellenreuther and Dr. Bengt Hansson,
Department of Biology, Lund University. This PhD project was also funded by the Department
of Biology, University of Copenhagen, and the field work conducted was supported by
National Park Thy and National Park Wadden Sea.

This thesis is comprised of a synopsis, four main chapters and two last sections. The synopsis
gives an overview of the background and objectives of the thesis and summarizes the main
aims and findings. The second part consists of four manuscripts in the form and scientific
papers. These chapters are the core part of the PhD thesis. Then follow two appendices.
Appendix I documents unfinished scientific work on topics related to the objectives of the
thesis and briefly describes non-scientific work such as courses, teaching and supervision, all
carried out during the PhD period. Last in appendix II is a published peer-reviewed paper on
the invasion history of Rosa rugosa based on my MSc thesis and subsequent work, which I
finished during my PhD period.

This thesis has an additional output which has not yet been produced: A report on
management initiatives and prioritization to the two Danish national parks, which kindly
offered staff and financial support during field work in 2012 and 2013. This report will be
based on the various findings documented primarily in the main chapters and to a lesser
extent, in the unfinished or undocumented work.

Andreas Kelager
Copenhagen, January 2015

Contents

Acknowledgement
English summary
Dansk resume

Synopsis 13
Introduction
Biotic interactions
Maculinea butterflies
The model system: Maculinea alcon and its two hosts
Environmental change: from global to local scale
Aim and paper synopsis
Overall conclusion and perspective
References
Chapter I 29
Host plant use drives genetic differentiation in syntopic populations of Maculinea alcon
Chapter II 53
Habitat suitability modelling of the rare diet specialist and ant brood parasitic butterfly
Maculinea alcon
Chapter III 79
Landscape genetics of the vulnerable social parasitic butterfly Maculinea alcon
Chapter IV 113
Biotic envelope modelling of a butterfly using two hosts suggests geographic stability under
future climate change
Appendix I 139
Unfinished scientific work
1. Comparative population genetics of Maculinea alcon and Gentiana pneumonanthe: from
local to continental scale in Europe
1.1. Development of SNPs for Gentiana pneumonanthe and preliminary
phylogeographic implication
1.2. Preliminary phylogeography of Maculinea alcon in Europe
2. Re-evaluating the national red list assessment of Maculinea alcon in Denmark
Courses
Teaching, supervision and student year production
1st Annual PhD Day 2012 @ BIO
Appendix II 161
Multiple introductions and no loss of genetic diversity in the Japanese rose, Rosa rugosa, in

Europe
Acknowledgement
Research is not an individual endeavour, and I’m indebted to a great number of people
who’ve, one way or another, been part of my life during my PhD period.

First and foremost, I want to thank my two supervisors Hans Henrik Bruun and David Nash
for embarking on this journey with me and their support, encouragement and freedom to
pursuit my own ideas, and our discussions on the many subjects in this thesis. Thank you both
for keeping my on track towards the end. Hans Henrik, thank you for the days in the field
where we collected samples, taught and talked about nature, Maculinea, Gentiana or plants in
general. I particularly want to emphasize my gratitude to you David, for introducing me to the
Maculinea butterflies, what wonderful and intriguing organisms they are.

I wish to express my sincere gratitude to Maren Wellenreuther and Bengt Hansson for
hosting me at Lund University and for the many lively discussions on landscape genetics. I
give a special thanks to you Maren, and to Damien, for housing me every week during my
commute to Lund. Please give my warmest regards and big Pteranodon-hugs to Tarka and
Linnea from me.

András Tartally, thank you for inviting me on board the ‘Transylvanian project”. It has been
an experience from which I’ve learned a lot and it gave me a unique insight into the Maculinea
world. Thanks to Jens-Christian Svenning and Peder Bøcher for sharing the TWI-data and
giving valuable comments along the way. Thanks to Miguel Geraldes for sharing a lot of
Gentiana pneumonanthe samples and for our discussion about phylogeography. I also thank
the many collaborators who partook in sampling for the landscape genetics and
phylogeographic studies that were cancelled at the end of my PhD.

I could not have completed my thesis without the competence (and often patience) of ArcGIS-
wizard Bjørn Hermansen. Thank you always having an open door, even at stressful times.
Our engaging discussions on beer brewery and farming gave extra flavour to the work
environment. I hope to bring the family to Brinkholm one day. Katie Marske and David
Nogues-Bravo, I picked your brains and you were always ready to give sound advice and
feedback on my many questions. I’m glad I could share the world of a socially parasitic
butterfly with you and I’m ever grateful for your inspiration!

To my 5 BSc students Ea Hørsving, Maria Mikkelsen, Daniella Humm, Joakim Lassen and
Lærke Johansen, I give a high five and well done. I’ve learned a lot of from all of you. Anders
I, Anders J, Anne, Charles, Ida, Jimmy, Karen, Lærke, Marie, Martin, Mette, Nikolaj,
Rebekka and Sasha from DN-SAK (Copenhagen student division of The Danish Society for
Nature Conservation), Lærke Erica Lundsten and Søren B. Rasmussen are all greatly
acknowledged for all their help in the field! I give a special appreciation to you Lærke for all
your hard and proficient work with the Maculinea alcon flyers for the national parks. Always
keep your peculiar, friendly and warm Jutlandish humour!

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I’ve had the pleasure of sharing office with owl and frog individual-based modellers Rikke
Jensen and Maj-Britt Pontoppidan (thank you for the title as main pollinator of the
Botanical Garden), with social evolutionist and drawing wizard Manwir Singh, ant
supercolonist Louise Pedersen and with termite symbiont metabolistic Rafael Rodrigues da
Costa (for a few months).

Nynne-Cecilie Kelager Schmidt read and gave invaluable comments to the summaries and
synopsis of this thesis and her effort is greatly appreciated! Jonas Geldmann, thank you for
the helpful comments and suggestions on appendix I and for spending your holidays reading
it. Please also give my apologies to Katharina 

I give virtual cake and coffee to the writing session group: Jonas Geldmann, Marie Dam,
Peter Søgaard Jørgensen and Erik Mousing.

Professor Jacobus J. Boomsma and Professor Carsten Rahbek are thanked for providing
funding for my PhD project as well as creating a wonderful and inspiring work environment in
the two respective research centres: Centre for Social Evolution and Center for
Macroecology and Evolution. Of course, to all my colleagues (none mentioned, none
forgotten) at CSE and CMEC, you will be sorely missed. Charlotte Olsen, thank you for the
lab-assistance, you really helped me out in a tight spot! Sylvia Mathiasen, you will always be
my lab-mother. I will truly miss your humour and strawberry cakes! To all the employees and
students at the Section for Ecology and Evolution: thanks for all the fish over the last 8
years!

The Danish National Research Foundation supported this PhD project. Field work was
partly supported by Thy National Park and Wadden Sea National Park.

Last, but certainly not least to my Bellis Nynne-Cecilie and two children Viola and Louis. You
have been the ground pillar in my life, securing my sanity, making me laugh and keeping my
world from falling apart. Nyns, thank you for sharing my mountain peaks and supporting me
in the valleys. It’s been hard on everyone, and I’m glad my journey is at an end… I’m coming
home!

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English summary
The obligate socially parasitic Alcon Blue butterfly (Maculinea alcon) uses the Marsh Gentian
(Gentiana pneumonanthe) as its initial host plant, on which caterpillars develop during the
first larval instars. In the last larval stage, M. alcon lives as a brood parasite in colonies of
specific Myrmica host ants by using chemical and acoustic mimicry to coerce the ant workers
to feed and nurture the caterpillar preferentially over their own brood. Maculinea alcon is
thus an extreme dietary specialist as absence of just one of the hosts precludes presence of the
butterfly and as a result it is highly sensitive to the ongoing environmental change caused by
humans. The main drivers for its decline are changed land-use and associated habitat loss or
fragmentation, and (in more recent times) drainage, increased eutrophication and lack of
appropriate management, but future climate change may further enhance the risk of
extinction. Maculinea alcon is selected as an umbrella for conservation and numerous aspects
of its biology has been studied extensively.

This thesis explores the spatio-temporal impact of the tight biotic dependence in this tri-
trophic interaction system and integrates the large body of research with novel methods such
as spatial population genetics and macroecological modelling.

The results presented in this PhD thesis suggest that inclusion of biotic interactions in
macrecological models may completely alter predictions of species’ response to
environmental change. The cross-methodological approaches offer new insight into the
conservation of Maculinea alcon and thus aid the future management of this unique butterfly.

In chapter I we found two syntopic populations of M. alcon to be genetically differentiated
caused by their host plant flower phenology, not differences in host ant use as expected, and is
an example of a genetic barrier operating on a temporal scale rather than spatial. In chapter
II, we developed habitat suitability models for M. alcon and G. pneumonanthe potentially
useful in locating undocumented populations and for improving management of them at the
landscape scale. In chapter III, we integrated a model from chapter II but did not find an
effect of landscapes resistance on gene flow between populations, independent of geographic
distance. Instead our study showed that populations of Maculinea alcon are likely very
sensitive to both past and current anthropogenic change and that conservation should focus
on preserving or establishing functional network of habitats to support viable
metapopulations. In chapter IV, we found that the suitability of M. alcon in Europe is likely to
be geographically stable because of its tight dependence on the climatically stable hosts,
contrary to what strict climate-based model suggests. In appendix I is a draft argument to
uplist the red status of M. alcon in Denmark to Endangered (EN) from Vulnerable (VU) based
on temporal trends in distribution data for the butterfly and its host plant.

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