Reproductive Altruism, Social Diversity And Host Association In Sponge-Dwelling Snapping

235 Pages·2017·5.97 MB·English

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Dissertations, Theses, and Masters Projects Theses, Dissertations, & Master Projects
2016
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Tin Chi Solomon Chak
College of William and Mary - Virginia Institute of Marine Science, [email protected]
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Chak, Tin Chi Solomon, "Reproductive Altruism, Social Diversity and Host Association in Sponge-Dwelling
Snapping Shrimps, Synalpheus" (2016). Dissertations, Theses, and Masters Projects. Paper 1477068130.
http://doi.org/10.21220/V5MK5Q
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Reproductive altruism, social diversity and host association in
sponge-dwelling snapping shrimps, Synalpheus

_______________________________

A Dissertation
Presented to

The Faculty of the School of Marine Science
The College of William & Mary in Virginia

In Partial Fulfillment
Of the requirements for the Degree of
Doctor of Philosophy
_______________________________

By

Tin Chi Solomon Chak
2016
APPROVAL SHEET
This dissertation is submitted in partial fulfillment of
the requirements for the degree of
Doctor of Philosophy
________________________________________
Tin Chi Solomon Chak

Approved by the committee, May 2016

________________________________________
J. Emmett Duffy, Ph.D.
Committee Chairman / Advisor
________________________________________
Jan McDowell, Ph.D.
________________________________________
Mark Patterson, Ph.D.
________________________________________
Jeffrey D. Shields, Ph.D.
________________________________________
Dustin R. Rubenstein, Ph.D.
Columbia University, New York
DEDICATION

To my wife, Belinda, my son Clayton, my parents James and Florence, and God.
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TABLE OF CONTENTS
DEDICATION ............................................................................................................................ iii
TABLE OF CONTENTS ............................................................................................................ iv
ACKNOWLEDGMENTS .......................................................................................................... vii
LIST OF TABLES .................................................................................................................... viii
LIST OF FIGURES ....................................................................................................................... x
AUTHOR’S NOTE ................................................................................................................... xiii
ABSTRACT ............................................................................................................................... xiv
Introduction ............................................................................................................................ 16
References ........................................................................................................................................ 21
Chapter 1. Social control of reproduction and breeding monopolization in the
eusocial snapping shrimp Synalpheus elizabethae .................................................... 25
Introduction ..................................................................................................................................... 27
Material and Methods ................................................................................................................... 31
Gonadal development of workers in wild colonies ........................................................................ 31
Experimental analysis of worker reproductive capacity and physical aggression .......... 33
Statistical analysis ........................................................................................................................................ 34
Results ................................................................................................................................................ 36
Gonadal development of workers in wild colonies ........................................................................ 36
Experimental analysis of worker reproductive capacity ............................................................ 36
Experimental analysis of physical aggression ................................................................................. 37
Discussion ......................................................................................................................................... 38
References ........................................................................................................................................ 42
Appendix A: Supplemental Tables and Figures ................................................................... 52
Appendix B: Supplemental Materials and Methods ............................................................ 59
Testing for morphological castes ........................................................................................................... 59
Estimating size of maturity ...................................................................................................................... 59
Creating vacant sponges as semi-natural habitats for shrimp ................................................. 60
Pilot experiment to determine optimal experimental duration .............................................. 61
Supplemental References ............................................................................................................ 62
Chapter 2 Reproductive skew drives patterns of sexual dimorphism in sponge-
dwelling snapping shrimps ............................................................................................... 68
Abstract ............................................................................................................................................. 69
Introduction ..................................................................................................................................... 70
iv
Material and methods ................................................................................................................... 73
Histology .......................................................................................................................................................... 73
Scanning electronic microscopy ............................................................................................................ 75
Reproductive maturity and sex ratios ................................................................................................. 76
Social structure .............................................................................................................................................. 77
Sexual dimorphism ...................................................................................................................................... 78
Results ................................................................................................................................................ 79
Reproductive maturity and sex ratios ................................................................................................. 79
Sexual dimorphism ...................................................................................................................................... 80
Discussion ......................................................................................................................................... 81
References ........................................................................................................................................ 86
Supplemental material and methods ...................................................................................... 98
Determination of size at maturity ......................................................................................................... 98
Discrepancy between results from SEM and histology ................................................................ 99
Reproductive maturity and sociality .................................................................................................... 99
Sex ratio and sociality .............................................................................................................................. 100
Supplemental references ........................................................................................................... 101
Supplemental figures .................................................................................................................. 102
Chapter 3 Evolutionary transitions towards eusociality in snapping shrimps
.................................................................................................................................................. 110
Abstract ........................................................................................................................................... 111
Introduction ................................................................................................................................... 112
Results .............................................................................................................................................. 116
Demographic clustering ......................................................................................................................... 116
Social transition ......................................................................................................................................... 118
Discussion ....................................................................................................................................... 119
Methods ........................................................................................................................................... 123
Collections .................................................................................................................................................... 123
Synalpheus phylogeny .............................................................................................................................. 124
Demographic clustering ......................................................................................................................... 126
Social transitions ....................................................................................................................................... 128
References ...................................................................................................................................... 130
Supplementary Information ..................................................................................................... 144
Demographic characteristics of intermediate species .............................................................. 144
Social transitions: supplementary analyses and results .......................................................... 144
Chapter 4 Group advantage in communal and eusocial snapping shrimps ... 158
Abstract ........................................................................................................................................... 159
Introduction ................................................................................................................................... 159
Materials and methods ............................................................................................................... 162
Geographic and effective host ranges ............................................................................................... 162
Relative abundance per sponge and sponge occupancy .......................................................... 163
Data partitioning ........................................................................................................................................ 164
Phylogenetic regressions ....................................................................................................................... 165
Results .............................................................................................................................................. 166
Discussion ....................................................................................................................................... 167
References ...................................................................................................................................... 168
Supplementary Materials .......................................................................................................... 178
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Net relatedness of host sponges ......................................................................................................... 178
Supplementary References ....................................................................................................... 178
Chapter 5 Host association of snapping shrimps in sponge holobionts .......... 180
Abstract ........................................................................................................................................... 181
Materials and methods ............................................................................................................... 185
Shrimp-sponge associations ................................................................................................................. 185
Similarity of bacterial communities between sponges ............................................................. 185
Phylogenetic relationships between sponges ............................................................................... 188
Phylogenetic similarity between Synalpheus species ................................................................ 190
Data Analysis ............................................................................................................................................... 191
Results .............................................................................................................................................. 193
Discussion ....................................................................................................................................... 195
References ...................................................................................................................................... 198
Supplementary Materials .......................................................................................................... 218
PCR primers ................................................................................................................................................. 218
Cophylogenetic analyses ........................................................................................................................ 218
Cophylogenetic results ............................................................................................................................ 219
Mothur analysis pipeline ........................................................................................................................ 223
Conclusions .......................................................................................................................... 225
Summary ......................................................................................................................................... 226
Broader Context ............................................................................................................................ 226
Outlook ............................................................................................................................................ 229
References ...................................................................................................................................... 230
VITA ........................................................................................................................................ 233

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ACKNOWLEDGMENTS
First of all, I thank my major advisor, Dr. J. Emmett Duffy, who is always encouraging,
enlightening and entertaining. I am indebted to Emmett’s mentorship and this dissertation
would not be possible if Emmett did not unreservedly let me use the data he amassed
over the years.
I am grateful for my committee members who were very supportive of my work: Dr. Jeff
Shields, who is so deeply knowledgeable; Dr. Jan McDowell, who I can talk with as a
friend; Dr. Mark Patterson, who is inspiring; and most importantly Dr. Dustin
Rubenstein, my future postdoctoral supervisor who guided me through my doctoral
development and always challenged me to think deeper. My gratitude also goes to Dr.
Bongkeun Song who has provided tremendous help with next-generation sequencing and
opened my door to microbial biology. Last but not least, a deep thank to Dr. Kristin
Hultgren, who has been encouraging and supportive of my research, and has had an
incredible influence on my research directions.
I thank members of the VIMS biodiversity lab including Dr. Jon Lefcheck, Paul
Richardson, Shelby Ziegler, Sally Bornbusch, Danielle Hall, and Mary Chang for their
company and assistance. I am also indebted to the technical assistance from Shelley
Sullivan on histology, and Heidi Brightman and Gail Scott on sequencing.
I thank my funding sources including the Lerner Gray Memorial Fund, Short Trust VIMS
GK-12 fellowship, Sigma Xi, the Smithsonian Tropical Research Institute, and VIMS.
Last but not least, I thank my wife Belinda for her care, prayer, sacrifice, and patience.
Her support allowed me to go wholeheartedly into my research. And I thank my son
Clayton who can boost my energy with a smile.

vii
LIST OF TABLES
Chapter 1. Social control of reproduction and breeding monopolization in the
eusocial snapping shrimp Synalpheus elizabethae.........................................................25
Table A1. Sex and maturation status of adult workers from five S. elizabethae
colonies from the demosponge Lissodendoryx colombiensis......................................52
Table A2. Gonadal development of the workers that had the most advanced
development in each group under three experimental treatments...............................53
Table A3. Gonadal development of the workers that had the most advanced
development in each group under three experimental treatments where workers had
initial gonadal development.........................................................................................54
Table B1. Results of regressions between fixed finger length of the mojar chela and
carapace length in three colonies of S. elizabethae......................................................63
Chapter 2 Reproductive skew drives patterns of sexual dimorphism in sponge-
dwelling snapping shrimps..............................................................................................68
Table 1. Proportions of mature females and males, sex ratios (ASR and OSR),
proportion of hermaphrodites (herm.) and eusociality index (E) in Synalpheus spp.
from histology and scanning electron microscopy......................................................92
Table 2. Results of multiple regressions estimating the effects of (a) sociality or (b)
eusociality index, carapace length and operational sex ratio on allometry ratio using
raw data and (c) phylogenetic contrasts in Synalpheus...............................................93
Chapter 3 Evolutionary transitions towards eusociality in snapping shrimps........110
Supplementary Table 1. Synalpheus colony characteristics and social
organizations..............................................................................................................146
Supplementary Table 2. Sampling locations for Synalpheus from eight Caribbean
countries.....................................................................................................................148
Supplementary Table 3. Average silhouette distances (s) from seven PAM analyses
i
(A - G) using different demographic variables and different pre-assigned numbers of
clusters (k)..................................................................................................................149
Supplementary Table 4. Cluster assignments (k = 3) of Synalpheus species from
seven PAM analyses (A - G) using different demographic variables........................150
Supplementary Table 5. Effects of social organizations on demographic variables in
Synalpheus.................................................................................................................151
Supplementary Table 6. Comparison of models of continuous trait evolution using 22
Synalpheus species that were unambiguously assigned to one of three clusters (pair-
forming, communal, and eusocial).............................................................................152
viii
Supplementary Table 7. Comparison of models of continuous trait evolution using 30
Synalpheus species with more than 5 colonies (pair-forming, communal, eusocial,
intermediate 1, and intermediate 2)...........................................................................153
Supplementary Table 8. Comparison of models of continuous trait evolution using 39
Synalpheus species including ones with less than 6 colonies (pair-forming,
communal, eusocial, intermediate 1, and intermediate 2).........................................154
Supplementary Table 9. Genbank sequence information for the Synalpheus species
used in phylogeny......................................................................................................155
Chapter 4 Group advantage in communal and eusocial snapping shrimps.............158
Table 1. Host ranges (effective and raw), geographic ranges, group size, relative
abundances per sponge, and sponge occupancies (mean proportion of individual
sponges occupied) for 34 Synalpheus species...........................................................172
Table 2. Results of MCMCglmm regressions to test the ecological advantage
associated with increasing group size in eusocial and communal Synalpheus snapping
shrimps.......................................................................................................................174
Chapter 5 Host association of snapping shrimps in sponge holobionts....................180
Table 1. Associations between Synalpheus species and sponges in tropical West
Atlantic.......................................................................................................................208
Table 2. Regression results in models predicting phylogenetic similarity of shrimp
pairs (shrimpPS).........................................................................................................209

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