islands, archipelagos, and beyond: population genetics and phylogeography of hawaiian coral reef ...

166 Pages·2012·4.17 MB·English

by  Derek Skillings

ISLANDS, ARCHIPELAGOS, AND BEYOND: POPULATION GENETICS AND
PHYLOGEOGRAPHY OF HAWAIIAN CORAL REEF ECHINODERMS

A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE
UNIVERSITY OF HAWAI‘I AT MĀNOA IN PARTIAL FULFILLMENT OF THE
REQUIREMENT FOR THE DEGREE OF

DOCTOR OF PHILOSOPHY
IN
ZOOLOGY
AUGUST 2012

By
Derek J. Skillings

Dissertation Committee:
Robert Toonen, Chairperson
Brian Bowen
Charles Birkeland
Andrew Taylor
Ronald Bontekoe
i
DEDICATION

This dissertation is dedicated to my wife, Melissa Kay Skillings.
ii
ACKNOWLEDGEMENTS
First, I would like to thank my committee members who provided essential guidance and
encouragement throughout my graduate career. Foremost, I would like to thank my advisor and
committee chair Rob Toonen. He has generously offered me a near endless supply of advice and
guidance, as he does for anyone who knocks on his door. He also gave me the flexibility and
encouragement needed to make getting two simultaneous graduate degrees possible. My
graduate career has been very unconventional, and Rob has supported me every step of the way. I
would like to thank Brian Bowen for giving me the structure I needed to succeed. Given my
tendency to get lost in an always increasing number of projects, I would have never finished in a
reasonable amount of time without his firm hand at setting deadlines and his enthusiastic
encouragement to meet those deadlines. Rob and Brian gave me the perfect balance of freedom
and focus that I needed to succeed. I would like to thank Chuck Birkeland for helping me to put
my work in the larger perspective of coral reef ecosystems. Chuck also encouraged my
philosophical and historical investigations into biology through insightful conversation; every
time I saw he seemed to have a valuable and important text that he wanted to give me for my
collection, many from his personal library. I would like to thank Andy Taylor for his critical eye,
for being able to see through the details to get at the heart of the problem. Andy first taught me
statistics, a field that I didn’t appreciate at first, but have since come to focus on greatly because
of his influence. Even though we have come to take different approaches to statistics, he has
always challenged me in a way that has made my thinking clearer and has made me a better
academic. Finally, I would to thank Ron Bontekoe for his dual service as a committee member
for my PhD and as my advisor for my philosophy MA. His insightful questions and critical
feedback have pushed my writing leaps and bounds ahead of where I thought it could be.
iii
Thank you to the facility, staff, and postdoctoral researchers at the Hawai‘i Institute of
Marine Biology and the University of Hawai‘i at Mānoa Zoology department. I would like to
thank: Matt Iacchei, Michelle Gaither, Jon Puritz, Joseph DiBattista, Mike Stat, Zoltan Szabo,
Greg Concepcion, Kim Andrews, Marc Crepeau, Steve Karl and the rest of the extended ToBo
lab for helpful discussions and support. I would especially like to thank Chris Bird, who spent
many hours teaching me the skills I needed to be a successful molecular biologist. This work was
made possible by the financial support of several agencies including: National Science
Foundation, Papahānaumokuākea Marine National Monument, Northwestern Hawaiian Islands
Coral Reef Reserve, University of Hawai‘i Art and Sciences Council, and the Jessie D. Kay
Fellowship.

iv
ABSTRACT
Genetic connectivity determines the evolutionary independence of populations and plays
a primary role governing intraspecies evolution. Patterns of genetic connectivity can also be used
to make inferences about macroevolutionary processes. For my dissertation I used mtDNA
sequences in phylogeographic and population level analyses to examine connectivity within and
between Pacific Archipelagos, utilizing four species of tropical echinoderms. First, I review and
prescribe non-lethal sampling techniques for use in genetic studies of many species of marine
invertebrates. Second, I showed that two species of sea cucumber, Holothuria atra and
Holothuria whitmaei, with a similar life history, species range, and habitat usuage cannot be used
as proxies for each other in order to predict phylogeographic patterns, degree of connectivity, and
population genetic structure within the Hawaiian Archipelago. Third, I examined the genetic
population structure of H. atra across the central tropical Pacific to show that despite its large
range, H. atra has hierarchical, fine-scale population structure driven primarily by between-
archipelago barriers, but with significant differences between sites within an archipelago. Finally,
I compared population genetic patterns in two congeneric brittle stars, Ophiocoma pica and
Ophiocoma erinaceous, across Hawai‘i and Central and Eastern Polynesia. I found contrasting
phylogeographic patterns in these two similar species, as was the case with H. atra and H.
whitmaei. Given the real-world constraints of limited time and money in marine ecosystem
management it would be ideal if model species could stand in as proxies for a host of similar
species. This dissertation shows that this ideal scenario is unlikely to be the case; similar life
histories and close phylogenetic relationships do not appear to predict population connectivity.
Generalizations based on a few representative taxa are unlikely to offer much in terms of
delineating boundaries for spatial management areas. Though a more inclusive multi-species
v
approach is bound to cost more in terms of time and resources, it should ultimately payout as
more informed, if complex, management.
vi
TABLE OF CONTENTS
Dedication ………………………………………………………………………………… ii
Acknowledgements ………………………………………………………………………... iii
Abstract …………………………………………………………………………………... v
List of Tables ……………………………………………………………………………... ix
List of Figures ……………………………………………………………………………... x
Chapter 1: Introduction …………………………………………………………………... 1
References ………………………………………………………………………... 5
Table ……………………………………………………………………………. 9
Chapter 2: It’s Just a Flesh Wound: Non-lethal Sampling for Conservation Genetics
Studies……………………………………………………………………...…………... 12
Abstract …………………………………………………………………………... 13
Introduction ………………………………………………………………………... 13
Methods ...………………..………………………………………………………... 15
Discussion ………………………………………………………………………... 20
Conclusions ……………………………………………………………………….. 23
Acknowledgements ……………………………………………………………….. 23
References ………………………………………………………………………... 25
Figure ..…………………………………………………………………………...... 27
Chapter 3: Contrasting Phylogeography of Two Coral Reef Sea Cucumbers, Holothuria atra and
Holothuria whitmaei ………………….…………………………………….. 28
Introduction ……………………………………………………………………... 29
Methods ……………………………………………………………………...……. 35
Results ……………………………………………………………………...……… 38
Discussion …………………………………………………………………...…… 42
Conclusions ……………………………………………………………………….. 46
References …………………………………………………………………...…… 47
Tables ……………………………………………………………………...……… 60
Figures …………...……………………………………………………...………… 65
Chapter 4: Gateways to Hawai‘i – Genetic population structure of the tropical sea cucumber
Holothuria atra ……………………………………………….…………… 68
vii
Abstract ………………………………………………………...………………… 69
Introduction ………………………………………………………………...……… 69
Methods ……………...……………………………………………………..……. 73
Results ……………………………………………………………………………... 78
Discussion ………………………………………………………………………… 82
Conclusions ……………………………………………………………………….. 88
Acknowledgments ………………………………………………………………… 89
References ………………………………………………………………………... 91
Figures ………………………………………………………...………………… 104
Tables ………………………………………………………………………...…… 106
Appendices ………………………………………………………………………... 110
Chapter 5: Contrasting Phylogeography Patterns in Two Pacific Brittle Stars, Ophiocoma
erinaceous and Ophiocoma pica …………..………………………………………...… 113
Introduction ………………………………………………………………...……… 114
Methods ……………...……………………………………………………..……. 119
Data Analysis ……………………………………………………………………... 121
Results ……………………………………………………………………………... 123
Discussion ………………………………………………………………………… 127
Conclusions ……………………………………………………………………….. 131
References ………………………………………………………………………... 132
Tables ………………………………………………………………………...…… 146
Figures ………………………………………………………...………………… 150
Chapter 6: Summary and Synthesis ………………..…………………...………………… 152
Summary ………………………………………………………………...………… 153
Synthesis ………...…...……………………………………………………..……. 155

viii
LIST OF TABLES
Chapter 3: Contrasting Phylogeography of Two Coral Reef Sea Cucumbers, Holothuria atra and
Holothuria whitmaei
Table 3.1 Molecular diversity indices and sample sizes ………..........…………… 61
Table 3.2 Pairwise F statistic comparisons ………………………………...…...… 62
Table 3.3 Pairwise D comparisons …………………………………………. 63
est_chao
Table 3.4 AMOVAs by region ……………………………………………………. 64
Table 3.5 Pairwise population migration rate estimates …………………………... 65
Chapter 4: Gateways to Hawai‘i – Genetic population structure of the tropical sea cucumber
Holothuria atra
Table 4.1 Molecular diversity indices and sample sizes ………………………… 107
Table 4.2 Pairwise D and F comparisons ……………………….……….. 108
est_chao ST
Table 4.3 AMOVAs for different population groupings ……………………….… 109
Table 4.4 Pairwise population migration rate estimates ………………..………… 110
Chapter 5: Contrasting Phylogeography Patterns in Two Pacific Brittle Stars, Ophiocoma
erinaceous and Ophiocoma pica
Table 5.1 Molecular diversity indices and sample sizes ………………………… 147
Table 5.2 AMOVAs by region …………………….…………………….……….. 148
Table 5.3 Pairwise D and F comparisons ……...……………………….… 149
est_chao ST
Table 5.4 Pairwise population migration rate estimates ………………..………… 150

ix
LIST OF FIGURES
Chapter 2: It’s Just a Flesh Wound: Non-lethal Sampling for Conservation Genetics Studies
Figure 1.1 Non-lethal sampling of a Crown of Thorns sea star (Acanthaster planci)
without removing the animal from the substrate …………………………………… 28
Chapter 3: Contrasting Phylogeography of Two Coral Reef Sea Cucumbers, Holothuria atra and
Holothuria whitmaei
Figure 3.1 Map of the Hawaiian Archipelago …..………………………………… 66
Figure 3.2 Haplotype network for Holothuria atra …………….……………….... 67
Figure 3.3 Haplotype network for Holothuria whitmaei …………….…………… 68
Chapter 4: Gateways to Hawai‘i – Genetic population structure of the tropical sea cucumber
Holothuria atra
Figure 4.1 Map of Central Pacific with major barriers and migration rates………. 105
Figure 4.2 Haplotype network …………………….………….…………………… 106
Chapter 5: Contrasting Phylogeography Patterns in Two Pacific Brittle Stars, Ophiocoma
erinaceous and Ophiocoma pica
Figure 5.1 Haplotype network for Ophiocoma erinaceous ……………………… 151
Figure 5.2 Haplotype network for Ophiocoma pica ………………...…………… 152

x