Some evolutionary and ecological implications of colour variation in the sea urchin Heliocidaris erythrogramma

(1)

by

Jane Growns B.Sc. Jt. Hons. (U.C.N.W., Bangor)

submitted in fulfi lment of the requirements for the degree of

Doctor of Philosophy

University of Tasmania Hobart

(2)

I hereby declare that this thesis contains no material which has been accepted for the award of any degree or diploma in any university and that, to the best of my knowledge and belief, the thesis contains no copy or

paraphrase of material previously published or written by another person, except where due reference is made i n the text.

(3)

TABLE OF CONTENTS

Page

ABSTRACT

ACKNOWLEDGEMENTS I I

CHAPTER

1

GENERAL INTRODUCTION 1

CHAPTER 2 THE POLYMORPHISM, ITS PIGMENTS AND

POSS IBLE GENETIC BASIS

7

2.1

INTRODUCTION

7

2. 2

DESCRIPTION O F THE POLYMORPHISM

9

2.3

METHOOS

14

2.3.1

C ombi nations of pigmentation

1 4 2.3.2

Identification of pigments from the

calcareous parts

1 6

2.3.3

Identification of echinochrome A and

histolo g y

1

7

2.3.4

Diet preferences among morphs

1 8 2.3.5

Colour change experiments

1

8

2.4

RESULTS

19

2.4.1

· V ariation in test and spine colours

19 2.4.2

Distrib ution of spinochromes among

phenotypes

22

2.4.3

Identification of naphth o q u i n o ne

p i g ments

2 5

2.4.4

C omposition of the dermal pigment

g ra n u les

3

0

2.4.5

Diet preferences among morphs

3

0

2.4.6

Colour change

3

0

2.5

DISCUSSION

_{3 3}

CHAPTER 3 TEMPORAL STABILITY OF MORPH FREQUENCIES 3

7

3 .1

INTRODUCTION

3

7

3.2

METHODS

39

(4)

TABLE OF CONTENTS (continued)

P age

3 . 3 . 1 Stability o f morph pro p orti o n s d uring

the study 4 2

3 . 3 . 2 Variation i n der m i s c o l o ur proportions

between size classes 4 9

3 . 4 DISCUSSION 6 1

CHAPTER ₄ GEOGRAPHICAL VARIATION IN MORPH

FREQUENCIES AND ENVIRONMENTAL

ASSOCIATIO N S

4 . 1 INTRODUCTION

4. 2 MATERIALS AND M ETHODS 4.2. 1 Collection of d ata 4 . 2 . 2 Analysis of data 4 . 4 RESULTS AND DISCUSSION

4.4. 1 Small scale geographic var iation i n

6 4 6 4 6 8 6 8 7 4 8 2

pro portions of m orphs 8 2

4.4.2 Distr ibution of m orphs over entire

study area 9 0

4 . 4 . 3 S p atial p atterns i n dermis co l o ur

. pro p ortio n s 9 9

4.4.4 Association between dermis and spine

co l o ur 9 9

4 . 4 . 5 R elatio nsh ips between d er m i s col o ur

and environ mental data 1 0 2

4.4.6 Evidence for processes affecting

p o p u l at i o n d i ffer entiation 1 0 7

4 . 4 . 7 Water currents within and b etween the

geographical reg i o n s 1 1 7

4 .5 GENERAL DISCUSSION 1 1 9

CHAPTER ₅ VARIATION BETWEEN MORPHS IN MORPHOLOGY,

MICROHABITAT, REPRODUCTION AND TUBE

FEET STRENGTH _{1 2 4}

5 . 1 INTRODUCTION 1 2 4

5.2 METHODS 1 2 6

(5)

TABLE OF CONTENTS (continued)

5.2.2 M icrohab itat and b ehaviou ral variation 5 . 2 . 3 Rep rod uctive cycle and i nvestment 5 . 3 . 4 Tube feet stre n gth experiment 5 . 3 RESULTS

5 . 3 . 1 Morphometries and meristics

5 . 3 . 2 M icro hab itat and behavioural variatio n 5. 3 . 3 Reprod uctive cycle and investm ent 5.3. 4 Tube feet stren gth experiment 5. 5 DISCUSSION

CHAPTER 6 G EN E RAL D I S C U S S I O N

R EFERENCES

A P P E N D I CES

Appendix I Labo rato ry breeding trials.

Appendix 2a Dermis co lour d ata for all s ites A ppendix 2b Morph data for all sites

Appendix 3 Environmental data for all sites

Appendix 4a M eans, standard errors and sample sizes for morphometric and meristic vari ables, for red and wh ite dermis urchins and poo led data from Ti nderbox

Appendix 4b Means, standard errors and sample sizes for morphometric and meristic variables, for red and white dermis urch i ns and poo led data

P age I 2 9 I 31

1 3 1 1 3 2 1 3 2 I 34 I 5 2 1 5 2 1 5 8

I 6 1

1 69

1 79 1 79 I 8 9 I 90 1 9 1

1 9 2

fro m Ling Reef. I 9 3

Appendix 4c Means, standard errors and sample sizes for morphom etric and meristic variables, for Fo rtesc ue Bay urch ins.

Appendix 4d Means, standard errors and sample sizes for morphom etric and meristic variables, for red and w hite dermis urch ins and pooled data fro m Cowrie Pt.

1 94

(6)

ABSTRACT

An investigation into the evolutionary and ecological i mplications of variation in the external colou ration of the sea u rchin Hefiocidaris erythrogramma was made. Two different pigment systems create a complex polymorphism; red g ranules of echlnochrome A i n the dermis occur i n varying densities, and purple and green naphthoquinone pigments are fou nd in the calcareous test and spines. Many morphs may occur within one population, but the proportions of morphs vary markedly between sites.

Evidence from the observed variability and chemistry of the pigments strongly indicates that the variation has a genetic basis. Breedi ng studies wh ich would have resolved this question were unsuccessful, but did show that all crosses between morphs developed and metamorphosed successfully.

Repeated sampling of 1 5 sites showed that morph propo rtions were stable at most sites ove r the 35 _{months of the study. Geographic variatio n i n the} proportions of morphs was determined from samples from 49 sites. Environme ntal

variables were recorded and the exposu re of each site to wave action was estimated using algal commun ities to develop an Algal Exposure Index (A. E . I . ) . Stepwise linear regression analysis i ndicated that the A.E.I. a n d amount of algal cover were the only environmental factors noted that we re useful predictor? dermis colour proportions.

Five hypotheses were developed (two selective and thre e stochastic) of processes which might be affecting morph proportions in the study area; these were tested using Mantel's non-parametric test. The results suggest that four geographical regions each ·have different patterns of morph distribution which are controlled by unique combinations of selection (re lated to exposure) and gene flow. These results are generally supported by what is known of water currents in each region, as most gene flow in H. erythrogramma will occur due to move ment of pelagic larvae.

(7)

ACKNOWLEDGEMENTS

I _{g ratefu lly acknowledge a l l the people t hq.t helped me i n the}

preparatio n of this thes is.

Peter Whyte, who suggested the p roject in the first p l ace.

Mike Ben nett, Paul C ramp, Mike Driessen, Andrew Flem i ng, lvor Growns, Premek Hamr, Lee Hamr, Rowan H ug hes, Paul H u mp h ries, Jea n Jackson, J ohn Kalish, Klobs, R o n M awbey, Peter M o o ney, S arah M u nks, M ark Nelson, Dominic O'Brien, Steve Reid, Sean R iley, D av id R itz, C ra ig S anders on, Andrew West, Pete r W hyte, Gus Yea rs ley a nd especia l l y Richard Holmes, who acted as diving partners and field assistants and w ithout w h o m this p roject would not h ave been possible.

Andrew Constable, for co l lecting the d ata from Port P h illip Bay for nie and for comments on part of the thesis.

R ichard H o l mes, Wayne Kell y, Ron M awbey, and Barry Rumbold, for technical assistance both in the f ield a nd in the l aborato ry.

The Tas m a n i an Departmen t of Sea Fisheries, for the use of their aq uari u m facilities.

Dr. Adrian Blackman, for the use of facil ities in h is labo rato r

y

and helping me understand the chem istry. C h arlie D ragar, w ithout whom I m ig ht not h ave su rvived the chem istry.

G len McPherson, Paul Humphries, Bob Bl ack, M ike Johnso n , Alastair

Richa rdson, and Kit Williams, for stat istical and co mputing he I p .

C raig S anderson, for help i n algal taxonomy and developing the A E I . Adrian Brad ley, f o r help with the histology.

Bob Black, Paul H u m p hries, M ike Johnson, and my supervisor, David R itz, for careful and constructive criticism of the m a n uscript.

I wo uld like to t ha nk the Depa rtment of Zoo logy of the Univers ity o f Western A ustralia a nd particu larly Bob Black and M ike Jo h ns o n for h osti ng me d u ring the writing of the thesis.

All my friends who supported and encouraged me, especially Sarah and Jean, Prem and Lee , and Humphries l suppose. Special thanks must go to lvor for m aking it a l l w o rthwhi le.