Variation in colonizer assembly sequence and intraspecific priority effects alter interspecific ...

210 Pages·2014·4.93 MB·English

Abstract
Intraspecific Variation in Metacommunities: Linking Regional
Heterogeneity to Local Population Dynamics
by
Christopher Joseph Dibble
Variation within species drives differences in population dynamics, interactions
between species, and the functioning of complex ecosystems. Fittingly, understanding the
factors that govern this intraspecific variation remains a central goal of ecology and
evolutionary biology. Local processes such as adaptation tend to increase divergence
among distinct populations, while regional processes such as dispersal and gene flow
tend to homogenize those differences. My research addresses how heterogeneity is
maintained despite the movement of individuals around a landscape. Specifically, I use
an experimental host-parasite system to propose and test mechanisms contributing to
ecological differentiation. Initially, I found that variation in colonizer traits makes the
order in which they arrive to a new habitat important. Intraspecific priority effects (IPEs)
occur when early arrivers limit the growth of late arrivers, and drive context-dependent
differences in growth among populations (Chapter 1). These effects of variation in
individual traits and arrival order extended to alter interspecific competition and
host/parasite interactions. My research indicates, then, that the process of community
assembly depends not only on the traits of a dominant species in the environment, but
also which individuals of that species get there first (Chapter 2). The relatively short-term
importance of IPEs, however, may wane over time as individuals continue to disperse
among populations. I tested the consequences of repeated dispersal, and found that they
depend heavily on the expected fitness of migrants in their new habitat. That is, dispersal
from a common source can increase ecological heterogeneity among populations if
migrants have different effects in different environments (Chapter 3). The context-
dependent effects of dispersal suggested an underlying trait-based mechanism.
Specifically, I hypothesized that the effects of increasing trait variance in a population
(e.g. via immigration) depend on the relationship between a population’s trait mean and
the local environmental optimum. I found that increasing trait variance helps populations
with suboptimal trait means, but harms populations already well-suited to the local
environment, doubling their disease burden (Chapter 4). Overall, my research identifies
novel ways in which intraspecific variation contributes to its own maintenance, limiting
the ability of individual movement among populations to homogenize ecological and
evolutionary differentiation.
Acknowledgments
More than any other factor, finding the right thesis advisor can make or break a
graduate career. Matching long-term interests, styles, expectations, and personalities
based on a relatively short courting period is a bit like proposing on the first date. I am
indebted to Dr. Volker Rudolf for his patience, mentoring, and example, in addition to
proving that you can excel in academia, have a family, and still be a nice person. Thank
you for taking a gamble.
I owe many thanks to my thesis committee, Dr. Tom Miller, Dr. Michael Kohn,
and Dr. David Lane, for their time, expertise, and thoughtful advice. Additionally, Dr.
Ken Whitney, Dr. Jenn Rudgers, and Dr. Hadley Wickham provided valuable feedback
on ideas and proposals during my early graduate career. I’d like to acknowledge the EEB
program at Rice for financial support, and for fostering a uniquely excellent environment
for teaching and research. Many of my most formative interactions occurred in casual
settings at the lunch table, in informal journal clubs, or on the steps of Valhalla. I owe a
great deal to the many exceptional graduate students, faculty, and post-docs I’ve been
fortunate enough to encounter during my time at Rice. Particular mention must go to Dr.
Ben Van Allen and Dr. Nick Rasmussen, who have each contributed immensely to my
research and thoughts on science (though they share no responsibility for my faults in
either). Dr. Volker Rudolf, Dr. Reed Cartwright, and Dr. Scott Solomon have greatly
improved my teaching, albeit in very different ways. Thanks also to Rice IACUC for not
caring about invertebrates. Many thanks to the EEB front office staff for sorting out all of
the problems I made for them. Diane Hatton, Laura Johnson, Rachel Stones, Lauren
Hanson, and Andrea Zorbas deserve special recognition.
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Special mention must also go to the Rudolf lab, without which much of this work
would not have been possible. Amber Roman deserves immense credit for running the
show for many years, and I have benefitted tremendously by interacting with and
mentoring some of the very gifted undergraduates to work in the lab. Specifically, Erin
Mattson, Erica Harris, Emily Crowder, Sena McRory, Kenna Fowler, and Jordan Bunch
deserve credit for their independent research, and Maya Carrillo and Jack Petersen were
priceless assets as Daphnia wranglers and yeast lancers.
I also owe a great deal to Dr. Meg Duffy and Dr. Spencer Hall, who introduced
me to the Daphnia – Metschnikowia system. Many, many thanks go to Spencer and his
students Alex Strauss, Dave Civitello, Jessica Hite, and Marta Shocket at Indiana
University. They hosted me for several summers’ worth of research, and are a fantastic
set of collaborators.
Thank you to my family, in-blood and in-law, for backing this odd five-year
decision. I’m sorry I haven’t visited more.
Last in mention but foremost in thought, thanks to my wife Sarah. Odd as it
seems, I never would have started this particular journey without your unwavering
support. I’m sorry for waiting so long to propose. I’m pretty sure I knew on our first date.
Table of Contents
Abstract ...................................................................................................................... i
Acknowledgments ..................................................................................................... iii
Table of Contents ....................................................................................................... v
List of Figures ............................................................................................................ ix
List of Tables ............................................................................................................. xi
Intraspecific priority effects and disease interact to alter population growth .............. 1
1.1. Abstract .................................................................................................................... 1
1.2. Introduction .............................................................................................................. 3
1.3. Methods ................................................................................................................... 5
1.3.1. Study system ...................................................................................................... 5
1.3.2. Experimental design .......................................................................................... 6
1.3.3. Infection assay ................................................................................................... 6
1.3.4. Mesocosm experiment ...................................................................................... 7
1.3.5. Statistical analyses ............................................................................................. 8
1.4. Results .................................................................................................................... 11
1.4.1. Microcosm infection assay .............................................................................. 11
1.4.2. Mesocosm experiment .................................................................................... 12
1.5. Discussion ............................................................................................................... 14
1.5.1. IPEs – the signature in population growth ...................................................... 15
1.5.2. Intraspecific priority effects – mechanisms ..................................................... 16
1.5.3. Ecological and evolutionary implications ........................................................ 19
1.6. Acknowledgements ................................................................................................ 20
1.7. Literature Cited ....................................................................................................... 21
1.8. Tables ...................................................................................................................... 26
1.9. Figures .................................................................................................................... 27
1.10. Appendix A ........................................................................................................... 33
Variation in colonizer assembly sequence and intraspecific priority effects alter
interspecific competition and disease epidemics ...................................................... 38
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2.1. Abstract .................................................................................................................. 38
2.2. Introduction ............................................................................................................ 40
2.3. Methods ................................................................................................................. 42
2.3.1. Study system .................................................................................................... 42
2.3.2. Experimental design ........................................................................................ 43
2.3.3. Statistical analyses ........................................................................................... 44
2.4. Results .................................................................................................................... 47
2.5. Discussion ............................................................................................................... 49
2.5.1. IPEs and intraspecific dynamics ....................................................................... 50
2.5.2. IPEs and interspecific dynamics ....................................................................... 51
2.5.3. Conclusions ...................................................................................................... 52
2.6. Acknowledgements ................................................................................................ 53
2.7. Literature Cited ....................................................................................................... 53
2.8. Tables ...................................................................................................................... 57
2.9. Figures .................................................................................................................... 59
2.10. Appendix A ........................................................................................................... 62
2.10.1. Raw growth data ............................................................................................ 63
2.10.2. Estimating Daphnia Population Growth: ....................................................... 64
2.10.3. Generalized linear mixed model results and summary statistics: ................. 66
2.10.4. Additional figures ........................................................................................... 70
Dispersal “type” and amount interact to affect ecological heterogeneity among local
populations .............................................................................................................. 72
3.1. Abstract .................................................................................................................. 72
3.2. Introduction ............................................................................................................ 74
3.3. Methods ................................................................................................................. 76
3.3.1. Study system .................................................................................................... 77
3.3.2. Initial infection assay ....................................................................................... 78
3.3.3. Experimental setup and dispersal treatments ................................................ 79
3.3.4. Statistical analyses ........................................................................................... 81
3.4. Results .................................................................................................................... 84
3.4.1. Host abundance ............................................................................................... 84
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3.4.2. Parasite dynamics ............................................................................................ 85
3.5. Discussion ............................................................................................................... 87
3.5.1. Effects on hosts ................................................................................................ 87
3.5.2. Effects on parasites .......................................................................................... 90
3.5.3. Role of dispersers ............................................................................................ 91
3.5.4. Conclusions ...................................................................................................... 93
3.6. Acknowledgements ................................................................................................ 93
3.7. Literature Cited ....................................................................................................... 94
3.8. Figures .................................................................................................................. 102
3.9. Appendix A ........................................................................................................... 108
The ecological and evolutionary effects of phenotypic variance depend on the
relationship between the mean phenotype and the environmental optimum ......... 113
4.1. Abstract ................................................................................................................ 113
4.2. Introduction .......................................................................................................... 115
4.3. Methods ............................................................................................................... 122
4.3.1. Initial clone isolation ...................................................................................... 122
4.3.2. Life table assay ............................................................................................... 124
4.3.3. Heritability and relationships among life table traits .................................... 126
4.3.4. Maintenance and re-acclimation of clones ................................................... 127
4.3.5. Individual infection assay .............................................................................. 127
4.3.6. Population infection assay ............................................................................. 129
4.3.7. Factorial manipulation of trait mean and variance ....................................... 130
4.3.8. Evolution of susceptibility.............................................................................. 135
4.4. Results .................................................................................................................. 136
4.4.1. Relationships among life history traits .......................................................... 136
4.4.2. Relationships between life history traits and disease risk ............................ 137
4.4.3. Factorial manipulation of trait mean and variance ....................................... 141
4.4.4. Effects on Daphnia abundance ...................................................................... 142
4.4.5. Effects on disease epidemics ......................................................................... 144
4.4.6. Evolution of susceptibility.............................................................................. 145
4.4.7. Results summary ............................................................................................ 146
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4.5. Discussion ............................................................................................................. 147
4.5.1. Daphnia traits and disease risk ...................................................................... 148
4.5.2. Factorial manipulation of trait mean and variance ....................................... 149
4.5.3. Mechanisms driving positive effects of increasing trait variance ................. 150
4.5.4. Mechanisms driving negative effects of increasing trait variance ................ 152
4.5.5. Trait evolution ............................................................................................... 154
4.5.6. Summary ........................................................................................................ 156
4.5.7. Conclusions .................................................................................................... 156
4.6. Acknowledgements .............................................................................................. 157
4.7. Literature Cited ..................................................................................................... 157
4.8. Figures .................................................................................................................. 172
4.9. Appendix A ........................................................................................................... 183
4.9.1. Life table assay ............................................................................................... 186
4.9.2. Individual and population assays................................................................... 190
4.9.3. Factorial manipulation of trait mean and variance ....................................... 191
List of Figures
Figure 1.1. a Infection prevalence in a laboratory-based infection assay for two lake
populations of a zooplankton host-grazer (Daphnia dentifera) used in the mesocosm
growth experiment ................................................................................................................... 27
Figure 1.2. Population growth of experimental populations of Daphnia dentifera
upon colonization of a new habitat patch ........................................................................... 29
Figure 1.3. GAMM-derived estimates of Daphnia abundance through time
(coefficient means +/- SE) for experimental populations, showing influence of early
and late arriver identity (Susceptible = S, Resistant = R) when parasites are present
or absent ..................................................................................................................................... 31
Figure 1.4. Resource decline (chlorophyll a, µg/L, log-transformed) between day 9
and day 16 .................................................................................................................................. 32
Figure 2.1. Daphnia abundance from days 5 to 25 for order of arrival
treatments, showing fit to Eq. (1) with b (peak abundance) estimates for each
treatment .................................................................................................................................. 59
Figure 2.2. a. Treatment means ± 1 SE for Daphnia population performance (b –
peak density, Eq. 1), by order of arrival treatment.......................................................... 60
Figure 3.1. Individual susceptibility to the fungal parasite Metschnikowia
bicuspidata among natural lake populations of Daphnia dentifera ............................ 102
Figure 3.2. A,B. Population density (individuals / L, mean ± 1 SE) for A) low-
susceptibility and B) high-susceptibility resident populations of Daphnia dentifera
experiencing different rates of dispersal .......................................................................... 103
Figure 3.3. Higher dispersal rates slightly increase synchrony in population
abundance among resident populations........................................................................... 105
Figure 3.4. The likelihood of parasite establishment depends on early host growth
(line and shaded region = binomial GLM ± 1 SE). ........................................................ 106
Figure 3.5. Average peak prevalence of M. bicuspidata epidemics in two different
resident D. dentifera populations (one with low individual susceptibility, one with
high individual susceptibility [e.g. Figure 3.1]) ............................................................. 107
Figure 4.1. Jensen’s inequality and phenotypic variance. .................................... 172