palaeoecological changes in populations of antarctic ice-dependent predators and their ...

183 Pages·2016·7.42 MB·English

by  Jane Younger

PALAEOECOLOGICAL CHANGES IN
POPULATIONS OF ANTARCTIC
ICE-DEPENDENT PREDATORS
AND THEIR ENVIRONMENTAL DRIVERS
Jane Younger
BSc (Nanotechnology) (Hons),
BAntSt (Hons)
Submitted in fulfilment for the requirements for the
degree of Doctor of Philosophy
Institute for Marine and Antarctic Studies
June 2015
DECLARATION OF ORIGINALITY
This thesis contains no material which has been accepted for a degree or diploma by the University
or any other institution, except by way of background information and duly acknowledged in the
thesis, and to the best of my knowledge and belief no material previously published or written by
another person except where due acknowledgement is made in the text of the thesis, nor does the
thesis contain any material that infringes copyright.
Jane Younger
22/06/2015
AUTHORITY OF ACCESS
The publishers of the papers comprising Chapters 1, 2, 3 & 4 hold the copyright for that content, and
access to the material should be sought from the journals, Global Change Biology (Chapters 1 &2)
and BMC Evolutionary Biology (Chapters 3 & 4). The remaining non published content of the thesis
may be made available for loan and limited copying and communication in accordance with the
Copyright Act 1968.”
CONTENTS
List of figures ............................................................................................................................... vi
List of tables ............................................................................................................................... vii
Abbreviations ............................................................................................................................ viii
Time periods referred to in text .................................................................................................... ix
Types of ice referred to in text ..................................................................................................... ix
Statement of ethical conduct ........................................................................................................ x
Statement of co-authorship ......................................................................................................... xi
Acknowledgements ................................................................................................................... xiii
Abstract ..................................................................................................................................... xvi
Map of Antarctica ...................................................................................................................... xix
Chapter 1 - A review of palaeoecological changes in Southern Ocean marine predator populations
and their environmental drivers .................................................................................................... 1
1.1 Introduction ................................................................................................................................... 2
1.2 An overview of Southern Ocean palaeoclimate............................................................................. 3
1.3 Palaeoecology of the Southern Ocean ........................................................................................... 7
1.4 Ice-free breeding species – the sub-Antarctic ............................................................................... 8
1.4.1 King penguins .......................................................................................................................... 9
1.4.2 Southern elephant seals .......................................................................................................... 9
1.5 Ice-free breeding species – the Pygoscelis penguins ................................................................... 13
1.5.1 Chinstrap penguins ................................................................................................................ 14
1.5.2 Gentoo penguins ................................................................................................................... 14
1.5.3 Adélie penguins ..................................................................................................................... 15
1.6 Ice-free breeding species – flying seabirds of the Antarctic continent........................................ 17
1.6.1 Snow petrels .......................................................................................................................... 17
1.7 Antarctic sea ice breeders ............................................................................................................ 18
1.7.1 Emperor penguins ................................................................................................................. 18
1.8.1 Weddell, crabeater and Ross seals ........................................................................................ 19
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1.9 Key long-term drivers of Southern Ocean predator populations ................................................ 20
1.10 Statement of thesis aims ........................................................................................................... 23
1.11 References ................................................................................................................................. 24
Chapter 2 - Too much of a good thing: sea ice extent may have forced emperor penguins into
refugia during the last glacial maximum ...................................................................................... 33
2.1 Abstract........................................................................................................................................ 34
2.2 Introduction ................................................................................................................................. 34
2.3 Methods ....................................................................................................................................... 37
2.3.1 Sample collection .................................................................................................................. 37
2.3.2 DNA extraction, amplification and sequencing .................................................................... 38
2.3.3 Data analysis – summary statistics and population structure .............................................. 40
2.3.4 Data analysis - demographic histories .................................................................................. 40
2.4 Results.......................................................................................................................................... 41
2.4.1 Present day population structure ......................................................................................... 41
2.4.2 Population history with respect to climate change .............................................................. 44
2.5 Discussion .................................................................................................................................... 46
2.6 References ................................................................................................................................... 51
2.7 Appendices .................................................................................................................................. 59
Appendix 2.1 Haplotype networks of phylogenetic relationships ................................................. 59
Appendix 2.2 Table of primer sequences. ...................................................................................... 60
Chapter 3 - Contrasting responses to a climate regime change by sympatric meso-predators ........ 62
3.1 Abstract........................................................................................................................................ 63
3.2 Introduction ................................................................................................................................. 63
3.3 Methods ....................................................................................................................................... 66
3.3.1 Sample collection .................................................................................................................. 66
3.3.2 Molecular laboratory ............................................................................................................ 68
3.3.3 Genetic diversity and present day population structure ....................................................... 68
3.3.4 Reconstructions of demographic history .............................................................................. 69
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3.4 Results .......................................................................................................................................... 70
3.4.1 Genetic diversity .................................................................................................................... 70
3.4.2 Extant population structure .................................................................................................. 71
3.4.3 Trends in effective female population size ............................................................................ 72
3.5 Discussion ..................................................................................................................................... 74
3.5.1 Ecological niche ..................................................................................................................... 74
3.5.2 Adaptive capacities ............................................................................................................... 77
3.5.3 Adaptive capacity and contemporary climate change .......................................................... 78
3.5.4 Concluding remarks ............................................................................................................... 79
3.6 References .................................................................................................................................... 80
3.7 Appendices ................................................................................................................................... 86
Appendix 3.1 Table of primer sequences........................................................................................ 86
Appendix 3.2 Table of summary statistics of Weddell seal and emperor penguin colonies by
genetic region ................................................................................................................................. 87
Chapter 4 - Rapid response of East Antarctic Adélie penguins to deglaciation ............................... 89
4.1 Abstract ........................................................................................................................................ 90
4.2 Introduction ................................................................................................................................. 90
4.3 Methods ....................................................................................................................................... 94
4.3.1 Field collections ..................................................................................................................... 94
4.3.2 Molecular laboratory ............................................................................................................ 94
4.3.3 Summary statistics ................................................................................................................ 95
4.3.4 East Antarctic demographic reconstructions ........................................................................ 95
4.3.5 Antarctic wide phylogeny ...................................................................................................... 96
4.4 Results .......................................................................................................................................... 97
4.4.1 Summary statistics ................................................................................................................ 97
4.4.2 East Antarctic Adélie penguin abundance over the past 22,000 years ................................. 98
4.4.3 Antarctic wide mtDNA phylogeny ......................................................................................... 99
4.5 Discussion ................................................................................................................................... 101
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4.6 References ................................................................................................................................. 105
Chapter 5 - RADSeq reveals a glacial refuge for emperor penguins at the Adare Peninsula .......... 111
5.1 Abstract...................................................................................................................................... 112
5.2 Introduction ............................................................................................................................... 112
5.3 Methods ..................................................................................................................................... 117
5.3.1 Sampling ............................................................................................................................. 117
5.3.2 Restriction-site-associated DNA sequencing (RADSeq) ...................................................... 118
5.3.3 Bioinformatics ..................................................................................................................... 118
5.3.4 Delimitation of genetic populations ................................................................................... 119
5.3.5 Genetic diversity ................................................................................................................. 120
5.3.6 Reconstructions of demographic history ............................................................................ 120
5.4 Results........................................................................................................................................ 122
5.4.1 RADSeq genotyping success................................................................................................ 122
5.4.2 Emperor penguin breeding populations ............................................................................. 122
5.4.3 Divergent individuals in the Weddell Sea ........................................................................... 127
5.4.4 Locations of glacial refugia ................................................................................................. 127
5.5 Discussion .................................................................................................................................. 130
5.5.1 Emperor penguin population structure and philopatry ...................................................... 130
5.5.2 Mystery migrants to the Weddell Sea ................................................................................ 133
5.5.3 Molecular markers for delimiting population structure ..................................................... 135
5.5.4 Glacial refugia ..................................................................................................................... 135
5.6 References ................................................................................................................................. 138
5.7 Appendices ................................................................................................................................ 144
Appendix 5.1 Extended Bayesian skyline plot trials to determine the optimal number of RAD loci
for analysis ................................................................................................................................... 144
Appendix 5.2 Principal components analysis ............................................................................... 145
Chapter 6 - Discussion ............................................................................................................... 148
6.1 Long-term vs. short-term drivers of population change ........................................................... 149
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6.2 Sensitivity to climate change ..................................................................................................... 150
6.3 Implications for the future of Adélie penguins, emperor penguins and Weddell seals ............ 152
6.4 Glacial refugia ............................................................................................................................. 154
6.5 Comparison of molecular markers for ecological studies .......................................................... 155
6.6 Future research directions ......................................................................................................... 156
6.7 References .................................................................................................................................. 157
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LIST OF FIGURES
1.1. The Antarctic temperature anomaly over the past 80,000 years …………………………...… …………. 4
1.2. Map of the Antarctic and sub-Antarctic with key physical features………………………..… …………. 6
1.3. Southern Ocean predator breeding distributions showing relevant environmental
features………………………………………………………………………………..……………………………………….. 10
2.1. Sample locations of emperor penguin colonies………………………………………………………… ……….. 37
2.2. Extended Bayesian skyline plots showing the change in effective female population
size………………………………………………………………………………………………..........................……….. 44
2.3. Phylogenetic relationships among individuals………………………………………………………..… ……….. 45
2.4. Schematic of contemporary population structure and reconstruction of historical
conditions…………………………………………………………………………………………………………………….... 48
3.1. Sampled colony locations and sea ice limits……………………………………………………………… ……….. 67
3.2. Population trajectories of East Antarctic Weddell seals and emperor penguins…….… ……….. 73
3.3. Post-glacial and Holocene environmental changes by sub-region compared to
abundance trajectories of Weddell seals and emperor penguins....................................... 75
4.1. Adélie penguin breeding distribution……………………………………………………………………..… ……….. 92
4.2. Abundance trend of East Antarctic Adélie penguins over the last 22,000 years…..…… ……….. 98
4.3. Phylogeny of Adélie penguins…………………………………………………………………………………… ….….. 100
5.1. Emperor penguin colony locations………………………………………………………………………….… ……… 113
5.2. RADSeq genotyping success……………………………………………………………………………………… ……… 124
5.3. Population assignment of individuals by Bayesian clustering……………………..………….… ……… 125
5.4. Trends in emperor penguin population sizes through time…………………………………….… ……… 131
5.5. Comparison of the demographic histories of colonies in the Ross Sea……………………… ……… 132
5.6. Victoria Land Coast of the north-western Ross Sea………………………………………………..… ……… 137
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LIST OF TABLES
1.1. Summary of Southern Ocean predator population changes reviewed.……..…………..……...…………... 22

2.1. Summary statistics by geographic and genetic region. ………………………………..……………………………… 42

2.2. Pairwise genetic differentiation between colonies ……………………………………………………………………… 43

3.1. Number of individuals sequenced by species and colony location..…………………………………………….. 66

3.2. Pairwise genetic differentiation (F ) between Weddell seal colonies.…………………………………………. 72
ST
3.3. Pairwise genetic differentiation (F ) between emperor penguin colonies…………………………….……. 72
ST
5.1. Number of individuals genotyped for each marker and colony.……………………………………..…………. 117

5.2. Pairwise genetic differentiation between colonies ……………………………………………………………..……. 126

5.3. Expected heterozygosity by population …………………………………………………………………….………………. 129
5.4. Pairwise comparisons of genetic diversity..……………………………………………………………………………….. 129
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ABBREVIATIONS
bp base pairs
BP Before physics (i.e. before 1950)
ca. circa
CytB mitochondrial gene cytochrome b
EAWS emperor penguin genetic population spanning East Antarctica and the Weddell Sea
EBSP extended Bayesian skyline plot
ESS effective sample size
F F-statistics
ST
gDNA genomic DNA
H expected heterozygosity
e
HPD highest posterior density interval
HVR mitochondrial hypervariable region
kya thousand years ago
Kyr thousand years
LGM last glacial maximum
MCMC Markov chain Monte Carlo
mya million years ago
Myr million years
N effective population size
e
N female effective population size
ef
RADSeq restriction-site-associated DNA sequencing
SD standard deviation
SNPs single nucleotide polymorphisms
Tau generation time
T time to most recent common ancestor
MRCA

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