Population structure and speciation in Begonia L.

199 Pages·2015·10.84 MB·English

Hughes, Mark (2002) Population structure and speciation in Begonia L.
PhD thesis

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Population structure and
speciation in Begonia L.
A thesis submitted to the University of Glasgow
for the degree of Doctor of Philosophy
Mark Hughes
Division of Environmental and Evolutionary Biology
June 2002
Declaration
I hereby declare that this thesis is composed of work carried out by
myself unless otherwise acknowledged and cited and that this thesis is of my
own composition. This research was carried out in the period of October 1998 to
June 2002. This dissertation has not in whole or in part been previously
presented for any other degree.
ABSTRACT
Biodiversityis unequally distributed between higher taxa; for example a
small n~mber of angiosperm genera contain the majority of angiosperm species.
Begonia is one of the largest angiosperm genera with ca. 1400 species. Studies of
such genera can give insights into the processess that cause diversification.
A number of features of the spatial distribution of biodiversity in Begonia
suggest gene flow between populations is poor and has affected larger-scale
patterns of diversity in the genus. These are (i) sporadic distribution of
populations, which are usually restricted to a specific micro-habitat, (ii) a high
degree of narrow endemism at the species level, (iii) widespread species being
rare and also highly morphologically variable unless they show atypical
adaptations that promote gene flow, and (iv) geographical restriction of
monophyletic groups.
Restricted gene flow betwee~ populations allows them to diverge in
response to weaker selection pressures than they would be able to respond to in
the face of gene flow from other populations. In order to examine population
structure (micro-evolution) in Begonia and its congruence to higher patterns of
diversity (macro-evolution), nuclear microsatellite markers have been isolated
and applied to two Begonia species, B. socotrana and B. sutherlandii.
Begonia socotrana is endemic to the Haggeher Mountains of the island of
Socotra in the Indian Ocean, where it has a total range of less than lOx 15 km.
PopUlation surveys have highlighted the need for its conservation status to be re
assessed, and it is proposed to reduce its status from 'endangered' to 'least
concern'. Population genetic analyses using microsatellite data show a significant
degree of population structure (Rsr 0.081, P<O.Ol; 9=0.096, P<O.Ol) and
significant isolation by distance, even over small spatial scales. The pattern of
isolation by distance could be due to restricted gene flow, or the result of small
. scale vicariance events in the fragmented peaks of the Haggeher Mountains
during climate change and resulting altitudinal migration.
Begonia sutherlandii is native to eastern and southern Africa, where it is
restricted to shaded, moist banks in indigenous forest. A high degree of
Population structure was found (9=0.482, P<O.OOl; RsrO.634, P<O.OOl), which
along with a high number of private alleles reflects the severe isolation of
populations in a patchily distributed forest habitat. Population relationships
appear to be strongly governed by the history and continuity of forest cover in
the region.
The population genetic studies of B. socotrana and B. sutherlandii show a
stnmg correlation of genetic variation with geography which reflect patterns seen
at larger scales. The correlation of micro and macro evolutionary patterns is
congruent with a hypothesis of restricted gene flow promoting speciation in
Begonia.
ACKNOWLEDGEMENTS
Without the philanthropy of the late Mr and Mrs Macintyre in setting up the
M.L. MacIntye Begonia Trusts, I would not have been able to spend three years
studying Begonia evolution. I am extremely grateful to them and to the trustees, in
particular Prof. Malcolm Wilkins and Dr. Chris Wheeler, for giving me this
opportunity.
My supervisor, Pete Hollingsworth, deserves thanks (and no doubt a drink)
for writing the initial project proposal and for guiding it through its subsequent
changes, and for reading through this entire thesis, giving helpful comments and
pointing out mildy amusing double entendres where relevant.
This research involved some interesting fieldwork, and I am grateful to
Tony Miller and Miranda Morris for organising the expedition to the Socotra
archipelago, which was no mean feat; Roger Hyam and Diccon Alexander for being
amiable travelling companions; and the people of Socotra for their hospitality and
for killing dozens of goats for us. My collecting trip in South Africa was assisted by
many people, particularly Tracy McLellan who provided air-conditioned transport
and company; Trevor Edwards and Christina Potgeiter who looked after me in
Pietermaritsburg when I arrived sans luggage and slightly the worse for wear from
in-flight tranquilisers; Chris Randle for driving to Tygerskloof; Tony Abbott for a
splendid stay in Umtamvuna, and Dirk Bellstedt for being a mine of information
and for getting me to some very interesting forest patches. I also received a great
deal of help on localities, transport and accomodation from the KZN parks board,
particularly Sharon Luow, Barry, Dennis Eckhart (contacts kindly given to me by
Michael Moeller), and Neil Crouch. Olive Hilliard and Bill Burtt also provided
helpful advice and maps during the planning of the trip.
The large amount of living material resulting from the fieldwork was
carefully tended to in quarantine by Fiona Inches and Andrea Fowler, apd
maintained in excellent condition upon its release by Steve Scott, Neil Watherston
and Fred Mobeck among others. Becky Govier patiently went through the mess that
was my collectors book and got most of it on BG BASE. The staff at Glasgow
Botanic Garden also deserve a mention for maintaining the national Begonia
collection, which made any trip through to Glasgow worthwhile.
This project also involved a great deal of labwork, which was made less of a
chore due to the excellent lab facilities at RBGE, provided by Michelle
Hollingsworth and Alex Ponge, who risked boredom and dermatitis in making up
the dozens of polyacrylamide gels I got through. Joanne Russell (SCRI) and Jane
Squirrell were both of great assistance in the tricky development of the
microsatellite markers. Ruth Hollands patiently dealt with the dozens of orders for
oligos and consumables. Thanks also to Jill Harrison for looking after me whilst I
invaded her bench space at Edinburgh University, and for being elsewhere when I
started a not inconsiderable fire in the PhD office. I would also like to thank
everyone in the lab and herbarium at RBGE for making it such a pleasant place to
work.
Assistance during the writing up phase came from many sources, including
Rod Page and Richard Ennos for providing data analysis advice, and Neil Brummitt
for heated debates on species-area relationships. All the RBGE library staff (in
particular Graham Hardy) have been very helpful in finding material and sorting
out copies and loans with spectacular efficiency. The latter stages of writing were
carried out whilst also working on a post doctoral project on Streptocarpus at
RBGE; Michael Moeller deserves a special mention for (i) employing me and (ii)
for being a very understanding boss during a busy time.
This project would not have been half as enjoyable were it not for the two
other Begonia students Laura Forrest and Vanessa Plana. Thanks especially to
Vanessa for knowledge of African Begonia, and to Laura for continuous and
welcome distraction by email, (including the odd academic one) and both for drinks
and good humour. I hope the two current Begonia students, Will Goodall
Copestake and Sophie Neale, enjoy their projects as much as I have.
Thanks also, of course, to my family and RG for their continuing support.
PREFACE
This thesis is an investigation of population structure in Begonia, and its
relevance to evolution and speciation in the genus. There are four introductory
chapters. The first is a general discussion of large scale patterns of biodiversity,
and possible causes for the unequal distribution of biodiversity between higher
taxa. The second is an account of the ecology and systematics of the
Begoniaceae, and aspects of Begonia biodiversity that may be of relevance to
popUlation structure and speciation processes. The third chapter is a discussion of
the effects of gene flow on population differentation and speciation, and the
fourth is a review of methods of analysing and interpreting population genetic
data obtained from micro satellite markers.
The next chunk of the thesis consists of five parts that are written as
papers intended for pUblication. As each is a complete paper in its own right, this
inevitably involves a small amount of repetition. The formatting for the
submitted papers in terms of tables, figures and references is according to the
format of the journal to which they were submitted. The first paper is a
monograph of two species of Begonia from the Socotra archipelago, and an
assessment of their conservation status. This has been accepted for publication by
the Edinburgh Journal of Botany. Papers two and three are technical papers
which describe the isolation and development of nuclear micro satellite markers
from two Begonia species, B. socotrana and B. sutherlandii. These have been
accepted for publication by Molecular Ecology Notes. The fourth paper is an
investigation of population differentiation and conservation genetics of Begonia
socotrana. This has been submitted to Biological Conservation. The fifth and
final paper is an account of the population structure of Begonia sutherlandii in
South Africa, and its relevance to broader scale patterns of biodiversity and
speciation in the genus as a whole. This paper will be submitted for pUblication
to Molecular Ecology. Each paper has its own self-contained reference list, and a
bibliography for the rest of the chapters is presented at the end of the thesis.
In the light of the findings of the preceeding chapters, the last chapter (5)
discusses the relevance of population structure and evolution in the Datiscaceae
(the sister family to the Begoniaceae) and in the angiosperms as a whole.
TABLE OF CONTENTS
CHAPTER 1. THE UNEQUAL DISTRIBUTION OF BIODIVERSITY
1.1. SOME TAXA ARE BIGGER THAN OTHERS 1
1.2. IS THE HOLLOW CURVE REAL OR IMAGINED?
1.3. CAUSES OF THE PATTERN 3
1.3.1. Stochastic and neutral models 3
1.3.2. Key innovations and adaptation 4
1.4. BEGONIA AS A LARGE GENUS 9
1.4.2. Why isn't Hillebrandia a large genus? 11
1.5. SUMMARY. 12
CHAPTER 2. THE BEGONIACEAE C. AGARDH.
2.1. INTRODUCTION TO THE BEGONIACEAE 13
2.1.1. Taxonomy and distribution 13
2.1.2. Ecology 14
2.1.3. Life cycle 16
2.1.4. Pollination biology 16
2.1.5. Dispersal biology 19
2.1.5.1. Fruit morphology andfunction 20
2.1.5.2. Seed morphology 20
2.2. THE DISTRIBUTION OF BEGONIA BIODIVERSITY AND
REASONS WHY INFREQUENT LONG DISTANCE GENE FLOW
MAY BE IMPORTANT IN BEGONIA SPECIATION 22
2.2.1. Species richness 22
2.2.2. Geographical monophyly 23
2.2.3. Narrow endemism 25
2.2.4. Rarity and variability of widespread species 28
2.3. SUMMARY 31
CHAPTER 3. GENE FLOW AND SPECIATION
3.1. INTRODUCTION 32
3.2. WITHIN-SPECIES GENE FLOW 33
3.3. SPECIATION CONCEPTS 35
3.3.1. Sympatric speciation 35
3.3.2. Geographic speciation 36
3.3.2.1. Parapatric speciation 36
3.3.2.2. Vicariant speciation 36
3.3.2.3. Peripheral isolate speciation 37
3.4. FREQUENCY OF SPECIATION MODES 37
3.4.1. Sympatric speciation 37
3.4.2. Geographic speciation 38
3.3.2.1. Parapatric speciation 38
3.3.2.2. Vicariant speciation 39
3.3.2.3. Peripheral isolate speciation 39
3.4.3. Evidence from phylogenetic data 42
3.5. GENE FLOW AND SPECIATION EMPIRICAL THEORY 43
3.6. SUMMARY 44
CHAPTER 4. MICRO SATELLITES AND DATA ANALYSIS
4.1. INTRODUCTION 46
4.2. MUTATION OF MICROSATELLITE SEQUENCES 46
4.3. FUNCTION OF MICRO SATELLITE SEQUENCES 49
4.4. ANALYSIS OF MICRO SATELLITE ALLELE DATA 50
4.4.1. F statistics and relatives 50
4.4.2. Genetic distanc;e measures
54
4.4.2.1.Geometric distances
54
A. Proportion ofs hared alleles
54
B. Fuzzy set similarity
55
C. Chord distance
55