The ontogeny and evolution of sexual dimorphism in paraclinin blennies (Teleostei: Labrisomidae).
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The ontogeny and evolution of sexual dimorphism in paraclinin blennies (Teleostei, Labrisomidae)
Brooks, Meriel Judith, Ph.D.
The University of Arizona, 1992
V·M·I 300 N. Zeeb Rd Ann Arbor, MI 48106
THE ONTOGENY AND EVOLUTION OF SEXUAL DIMORPHISM
IN PARACLININ BLENNIES (TELEOSTEI, LABRISOMIDAE)
by
Meriel judith Brooks
A Dissertation Submitted to the Faculty of the
DEPARTMENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY
In Partial Fulfillment of the Requirements For the Degree of
DOCTOR OF PHILOSOPHY
In the Graduate College
THE UNIVERSITY OF ARIZONA
1992 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE
As members of the Final Examination Committee, we certify that we have read
the dissertation prepared by ___M_e_r_~_'e_l __ J_u_d_~_'t_h __ B_r_o_o_k_S ______
entitled The Ontogeny and Evolution of Sexual Dimorphism in Paraclinin Blennies (Teleostei, Labrisomidae).
and recommend that it be accepted as fulfilling the dissertation requirement
for the Degree of Doctor of Philosophy ------~------
Date
Date
Date
Final approval and acceptance of this dissertation is contingent upon the candidate's submission of the final copy of the dissertation to the Graduate College.
I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement.
Dissertation Director 3
STATEMENT BY AUTHOR
This dissertation has been submitted in partial fulfillment of the requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the library.
Brief quotations from this dissertation are allowable without special permisSion, provided that accurate acknowledgement of source is made. Requests for permission for extended quotation from or reproduction of this manUScript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her jUdgement the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author. SIGNED: tVOu·gp ~Ilel-; # &k. 4
ACKNOWLEDGMENTS
Three people at the University of Arizona, Rich Strauss, Don Thomson, and Michael Donoghue, have influenced the direction my research has taken. I owe each for his unique contribution to this work. Don Thomson first introduced me the magnificent Sea of Cortez and the blennies that are so abundant there. Exploring one species of blenny, Paraclinus sini, led me to question the significance of sexual dimorphism in these fishes. In the first class Michael Donoghue taught at the U of A, phylogenetic systematies, I realized the importance of a phylogenetic framework for understanding the presence of dimorphism. My study of one species thus became the study of twenty one species. However, in order to compare dimorphism among species I needed a way to describe and quantify it. Rich Strauss introduced me to the intricacies and pitfalls of measurement, multivariate analyses, modeling and computer programming. For me, his ability in conveying not just the analytical methods of morphometries but their subtle beauty, expanded my world in previously unexplored directions. My strongest work is a direct result of his influence. Rich's enthusiasm is contagious; he is truly a gifted teacher.
I thank Dave Vleck and Bob Smith for serving on my committee, for being willing to read and comment when I asked for such help. When I first approached Dave to be on my committee he indicated that he could not help much, given the direction of my research. I have found that he, more than anyone, has a talent for pOinting out (usually with a question or two) exactly where I was indulging in foggy thinking.
Phil Hastings has been a steady guiding influence throughout my studies. He has always been available with ichthyological expertise and allowed me use of his computer when no others were available. Thanks Phil. Many fellow graduate students have contributed through discussion or emotional support. Foremost among these are Janet Voight, Michael Brogan, and Frank Cipriano. Without them, life in The Basement would not have been as full.
I am indebted to the following curators for loan of specimens, without which this work would not have been possible; R.A Rosenblatt, Scripps Institution of Oceanography; B. Chernoff, Field Museum of Natural History; D. Thomson, University of Arizona; W. Eschmeyer, California Academy of Sciences; C. Gilbert, Florida Museum of Natural History; V.G. Springer, National Museum of Natural History; Dr. Smith-Vaniz, Academy of Natural Sciences of Philadelphia, and D. Lavenberg, Natural History Museum of Los Angeles County.
Financial help for research and travel has been provided by the Department of Ecology and Evolutionary BiolOgy, the Graduate College, and the Research Training Group, University of Arizona; the Field Museum of Natural History; and Sigma-Xi Grants-In-Aid of Research.
This dissertation is dedicated to Melanie, Christopher, and Bob, none of whom typed the manUScript but all of whom smiled and nodded when I excitedly reported the results of new analyses. 5
TABLE OF CONTENTS
LIST OF ILLUSTRATIONS ...... 8
LIST OF TABLES...... 11
ABSTRACT ...... 12
GENERAL INTRODUCTION ...... 13
CHAPTER ONE: MODELING THE ONTOGENY OF SEXUAL DIMORPHISM
Abstract ...... 15
Introduction ...... •...... 16
Materials and Methods ...... 16
Growth Models...... 16
Case Study ...... 18
Background ...... 18
Material Examined ...... 18
Measurements ...... 19
Determination of General Size ...... 21
Sexual Dimorphism and Size ...... 21
Fitting the Models ...... 22
Results ...... 23
Pattern of Dimorphism ...... 23
Pattern of Allometric Growth ...... 24
Size-Independent Shape Differences ...... 27
Discussion ...... 27 6
Table of Contents (Continued)
CHAP1ER TWO: PHYLOGENETIC RELATIONSHIPS OF THE TRIBE PARACLININI (BLENNIOIDEI:LABRISOMIDAE)
Abstract ...... 36
Introduction ...... 36
Materials and Methods ...... •...... •...... 37
Taxa examined ...... 37
Outgroups and Polarity assessment ...... 37
Ingroup taxa...... 41
Characters ...... 41
Analyses ...... 64
Results and Discussion ...... 64
CHAP1ER THREE: EVOLUTION OF SEXUAL DIMORPHISM
Abstract ...... 84
Introduction ...... 84
Materials and Methods ...... 85
Measurements ...... 85
Material examined ...... 85
Allometric models ...... 85
Measuring sexual dimorphism ...... 86
Multivariate analyses ...... 87
Character evolution ...... 87
Results and Discussion ...... 90
Summary Tables ...... 90 7
Table of Contents (continued)
Selected Characters: Dimorphism, Ontogeny and Evolution ...... 94
Shape Differences Among Species ...... 125
Within Species Discriminate Analyses ...... '...... 125
Multivariate Analysis of Allometries ...... 131
CONCLUSIONS ...... 141
APPENDIX ONE: Description of Landmark Points...... 144
REFERENCES ...... 145 8
LIST OF ILLUS1RATIONS
1. Allometric growth models •...... 17
2. Mensural characters analyzed in Paraclinini ...... 20
3. Dimorphism patterns of four Paraclinus species ...... 25
4. Ontogenetic growth patterns of four Paraclinus species ...... 28
5. Discriminate plot of males, females, and juveniles for four Paraclinus species ...... 29
6. Anterior anal pterygiophore arrangement in five blennioids ...... 39
7. Relationships among blennioids based on allozyme data ...... " 40
8. Dorsal pterygiophore placement; possible character states ...... 48
9. Dorsal pterygiophore placement in outgroup taxa...... 49
10. Dorsal fin shape variation within Paraclinini ...... 50
11. Caudal skeleton characters and character states ...... 52
12. Pelvic fin characters ...... 53
13. Opercular spine characters ...... 54
14. Variation in suborbital bones ...... 56
15. Basisphenoid, pterosphenoid, and ventral postcleithrum ...... 57
16. Lateral process of hyomandibular ...... 59
17. Maxilla length variation within Paraclinini ...... 60
18. Head pore canal terminology used...... 61
19. Head pore variation ...... 63
20. Anal fin membrane posterior attachment ...... 65
21. Four 154 step cladograms ...... 67
22. Consensus of the four 154 step cladograms ...... 69
23. Strict, majority rule, and Adams consensus of 86 155 step trees ...... 70 9
List of illustrations (continued)
24. Consensus of all 161 step trees for inclusive taxa set ...... _ ...... _ . . .. 71
25. Consensus of unreoted analysis of all Paraclinini ...... 73
26. Possible relationships for P. magdalenae, P. ditrichus, and P. stephensi ...... _ . . .. 74
27. Mappings of six characters which show less homoplasy under topology 1 .... _ . . .. 76
28. Mappings of four characters shOwing less homoplasy under topology 2 ...... 77
29. Mappings of six characters which support clade 3 ...... _. 80
30. Mappings of four characters supporting subgroups of clade 3 ...... 81
31. Head and dorsal fin shape in clade 3 ...... 82
32. Maxilla length states mapped onto cladogram ...... 95
33. Diversity of jaw size in Paraclinini males ...... 96
34. Change in adult dimorphism as a result of acceleration in juveniles ...... _ . . .. 99
35. Pre- and post-displacement of size at allometric shift ...... _. 100
36. Male and female asper and marmoratus ...... 101
37. Juvenile asper and naeorhegmis ...... 103
38. Maxilla width mapped onto cladogram ...... 104
39. Scatterplots of maxilla width vs size for three species ...... 105
40. Slope differences for jaw characters among species ...... 106
41. Lateral measures of head length mapped onto cladogram ...... _ . .. 108
42. Dorsal measures of head length mapped onto cladogram ...... 109
43. Summary of total head dimorphism in Paraclinini ...... 111
44. Summary of scaled dimorphism index for Paraclinini ...... 113
45. Selected midbody dimorphic characters mapped onto cladogram ...... 114
46. Summary of total midbody dimorphism in Paraclinini ...... 116
47. Selected posterior body dimorphiC characters mapped onto cladogram ...... 117 10
List of illustrations (continued)
48. Summary of total posterior body dimorphism ...... 119
49. Selected dorsal fin dimorphic characters mapped onto cladogram ...... 120
50. Logtransformed dorsal spine lengths planed against general size ...... 122
51. Summary of total dorsal fin dimorphism ...... 123
52. Summary of total dimorphism, all body regions ...... 124
53. Plot of major Paraclinini clades on PCZ vs PC3 ...... 126
54. Discriminate plot of sexes for 5 species ...... 127
55. Discriminate plot of sexes for 3 primitive species ...... 128
56. PC plots of character allometries ...... 132
57. PC plot of head allometries; groups analyzed together ...... 134
58. PC plots of head allometries run for males females and juveniles separately ...... , 135
59. PC plot of body allometries for all groups ...... 137
60. PC plots of body allometries for males, females, and juveniles separately ...... 138
61. PC plot of dorsal fin allometries, for all groups ...... 139
62. PC plot of dorsal fin allometries clades 1, 2, and 3 indicated ...... 140 11
LIST OF TABLES
1. Summary of divergence pattern for four Paraclinus species ...... 26
2. Character correlations with DF1 ...... 30
3. Material examined ...... 42
4. Characters and character states ...... 44
5. Data matrix used for phylogenetic analysis ...... 66
6. CIs for characters under the two main tree topologies ...... 75
7. Pattern of sexual dimorphism...... 88
8. Pattern of ontgenetic divergence ...... 91
9. Species names abbreviations ...... 93
10. Character correlations with DF1 ...... 129 12
ABSTRACT
Ontogeny of sexual dimorphism within the Paraclinini is quite complex both within and among species. Differential growth in males is not the main cause of adult dimorphism. Rather, allometric shifts in both sexes produce adult shapes with approximately equal frequency. A trait that appears exaggerated in one sex is not always' produced ontogenetically by acceleration in growth of that trait. Larger male head size, for example, may rf'!sult from neoteny in females
(relative to juveniles) as often as acceleration in male growth. Females, rather than lOOking like large juveniles, are actually more different in shape from juveniles than are males. On this time scale then, females should be considered the divergent sex.
Phylogenetic analysis revealed three main lineages within the tribe. These groups are probably stable, though positions of some of the other species may change as more data become available. The most primitive species are grandicomis, nigripinnis, and cingulatus. The position of
Exerpes within the clade indicates that its single species should be included in the genus
Paraclinus.
Fairly extreme sexual dimorphism within Paraclinini seems to be the ancestral condition and has been variously modified within the clade. The trend is toward less extreme male and female difference with occasional reversal of a dimorphiC character. The decrease in amount of dimorphism seems to have occurred primarily through neoteny (relative to ancestral allometry), acceleration, and post-displacement. Juvenile growth has also changed relative to ancestral juveniles, affecting of adult as well as juvenile proportions. These evolutionary changes are independent of and in no way reflect the ontogenetiC paths producing dimorphism within a species. 13 GENERAL INTRODUCTION
Sexual dimorphism, although necessarily a property of both sexes (one sex cannot be different except in relation to the other) has historically been treated as a problem of male divergence. Males are viewed as different in evolutionary time, where differences are contrasted with ancestors (Shine 1989, Moore 1990), as well as in ontogenetic time, where differences are contrasted with female and juvenile growth and form (Stephens 1963, Cheverud and Richtsmeier
1986).
Growth patterns (allometries) of dimorphic characters are commonly assumed to change only in males at the onset of maturity, resUlting in male divergence in body form with increasing size. Stephens (1963) sums up a widespread belief with his statement "In most fishes that show dimorphism, the true dimorphic change takes place only in the mature male, while the female continues along the (growth) pattern already established". That males are diverging ontogenetically should be tested rather than assumed. Juvenile growth patterns provide the appropriate standard against which male and female growth should be compared. In Chapter
One I present three models for testing hypotheses of sex-specific allometric change, with an example of their application in four labrisomid blenny species. I use discriminate analysis of shape measures to investigate the commonly held belief that in dimorphiC species, shapes of adult females most closely resemble those of juveniles, with males extremely different from both.
The view of males as ontogenetically divergent from juveniles and females is paralleled by a view of males as evolutionarily divergent, and often the two are confused. Cheverud and
Richtsmeier (1986), for example, characterize females ontogenies as representing the ancestral condition. Again, it is possible that female ontogenies reflect ancestral growth, but it cannot be assumed that this is the case. Evolutionary change must be measured relative to a hypothesized ancestral condition. This can be achieved if one knows the phylogeny for a group of sexually 14 dimorphic species as well as the growth patterns within the group. Chapter Two summarizes the results of a phylogenetic analysis of labrisomid blennies, tribe Paraclinini. Sexual dimorphism varies among the twenty-one species comprising the tribe and there is evidence for this tribe's monophyly.
With the phylogenetic hypothesis from Chapter Two, I address in Chapter Three the question of divergence from the ancestral form and growth. Comparison of current growth patterns among the species with hypothesized ancestral growth patterns allow me to assess how often similar dimorphisms have evolved in this group and whether such dimorphism seems to have evolved under sexual selection and male divergence, selection for ecological divergence of both sexes, selection on another life stage altogether, or if species are dimorphic simply because the ancestor was dimorphic. 15
CHAPTER ONE
MODELING THE ONTOGENY OF SEXUAL DIMORPHISM
ABSTRACT
Studies of sexual dimorphism commonly focus on male morphology, often viewing males as divergent both evolutionarily and ontogenetically. For example, in continuously growing venebrates such as lizards and fishes, it has been assumed that adult dimorphism arises from growth rate changes in male characters at the onset of maturity. However, there has been little explicit treatment of the ontogenetic origin of morphological sex differences. I present here a method for testing hypotheses of sex-specific allometric change, and offer an example of its application in four species of labrisomid blennies. I develop three hierarchical models to test for allometric divergence: (1) the null model, in which adult allometries of both sexes are simply an extension of the juvenile allometries (model A); (2) a model in which either adult males or females (but not both) diverge from the juvenile trajectory (model B); and (3) a model in which adults of both sexes diverge from the juvenile allometry (model C). Growth that fits either of the two latter models results in shape dimorphism. While size dimorphism may occur in all three cases, it is not explicitly treated here. The models were tested with size series of four species of fish (Paraclinus, Labrisomidae). To further explore overall shape similarity among males, females, and juveniles, a multivariate analysis of shape (independent of size) was applied. Analysis of 42 mensural characters showed that divergence from juvenile allometry occurred as frequently in female traits as in male traits. Multivariate analysis showed that in all four species, female shape diverges more from juvenile shape than does male shape.
In addition, Similarity among adult dimorphic character states often resulted from quite different growth patterns, suggesting that resemblance of adult characters among related species is insufficient evidence to conclude character homology. Interpretations of sexual dimorphism, 16
currently emphasizing male morphology, may be biased and may underestimate the importance of selection on the female form as a cause of sexual dimorphism.
INTRODUCTION
Sexual dimorphism is an intraspecific phenomenon in which males and females differ in secondary sex characters. Many organisms which are sexually dimorphic at maturity are monomorphic during juvenile life stages, and sexual dimorphism in shape must result from shifts in relative growth rates as maturity approaches. In fishes, allometries of dimorphic characters are commonly assumed to change only in males at the onset of maturity, resulting in male divergence in shape with increasing size. For example, Stephens (1963) stated "In most fishes that show dimorphism, the true dimorphic change takes place only in the mature male, while the female continues along the pattern already established." This generalization has remained largely untested (but see Vitt and Cooper, 1985; Vial and Stewart, 1988; Cooper and
Vitt, 1989). In this study I propose three allometric models to determine whether shape dimorphism in mensural characters is a result of shifts in allometric trajectories of males, females, or both sexes. As an illustration I then apply this method to four congeneriC fish species (Paraclinus, Labrisomidae).
GROWTH MODELS
Shape change during growth can be evaluated as a change in the size of a character relative to a change in overall body size (the assessment of which is discussed below). Among males, females, and juveniles, growth may follow many possible trajectories. A hierarchical set of trajectory models was used in this study (Fig. 1), all based on the assumption that juvenile trajectories are identical for both sexes. The null model (model A) 17
Model A: 1 / Model A: 1 ... ~0 ~0 .. Monomorphic 1 ~~ ./ Dimorphic 1 '0~ ••••• ~0 / ... eD I I '0~ ./...... u;N 1 1 ~0 ... / ~ ./ cD 1 / 1 '0 / III 1/ 1/ Cii .c (J Cl 0 .~-I 1 \u-l0 1 ...J yf I I 1 ~I
Model 8 Model 8
! ...- ...-" ~0 •••••••••••••••••• 1 ~0 •••• '0~ .... 1 ~'I>", ...... 1 '~••••••• .. 1 .... It\a\e ------I .... _-- male 1·:::"'-- iU-./e(\\\e~
~ !1
Model C: Model C: 1 I /' Monomorphic Dimorphic 1 /' CD /' N I ~0 /' u; 1 ~/' a; '0 1 /' til Cii I /'/' female .c I.) ~-.... -.. -.-- Cl o ...J
I x X General size General size
Figure 1. Three models, A, B, and C used to evaluate character growth. In Model A all groups follow the same growth trajectory, resulting in no sexual dimorphism in shape. Alternately, either maturing males or females may diverge from the juvenile to adult trajectory (Model B) or both males and females diverge (Model C). 18 represents the case in which adults of both sexes continue along the juvenile growth trajectory.
In this case, the character is considered to be monomorphic in shape. When the sexes differ in
absolute body size (Fig. 1, model A, right), allometric growth may result in apparent shape
dimorphism. This apparent shape dimorphism is solely attributable to size differences between
the sexes, not to allometric shifts in males or females, and is not explicitly treated in the
models presented here. The second model (model B) represents the case in which one sex,
either male or female, continues along the established trajectory while the other diverges from
the juvenile trajectory. In the third model (model C), both sexes diverge from the juvenile
pattern. Males and females may diverge from the juvenile allometry with the same slope, in
which case the character is monomorphic, or with different slopes, in which case the character
is dimorphic (Fig. 1, model C, left and right respectively).
CASE STUDY
Background
The genus Paraclinus contains 20 nominal species of Neotropical labrisomid blennies
that vary in expression of sexual dimorphism. Reported dimorphism within Paraclinus includes
a longer maxilla and greater interorbital width in males, and a dorsal-fin incision and greater
pelvic to anal-fin distance in females (Hubbs, 1952; Springer, 1955; Rosenblatt and Parr,
1969).
Material Examined
Choice of species for this study was based on the availability of the appropriate size
range and number of specimens. Four Paraclinus species were selected: Paraclinus mexicanus
Gilbert, Paraclinus fasciatus Steindachner, Paraclinus sini Hubbs, and Paraclinus nigripinnis
Steindachner. Specimens from the holdings of The University of Arizona (VA), The Academy
of Natural Sciences of Philadelphia (ANSP), and Scripps Institution of Oceanography (SIO) 19 were examined: P. sini (N = 19 females, 16 males, 13 juveniles; UA 73-50); P. mexicanus (N =
17 females, 16 males, 8 juveniles; VA 69-48-22,69-42-2,68-68-6, 69-46-25); P. fasciatus (N =
15 females, 16 males, 11 juveniles; ANSP 93972; SIO 67-87-61); P. nigripinnis (N = 16 females,
16 males, 11 juveniles; ANSP 94623, 94618, 143116; SIO 67-87-61).
Measurements
Measures were taken from the maximum available size range of males, females, and juveniles to ensure that regression of a particular character against a general size axis would represent a complete ontogenetic trajectory (Cock, 1966; Leamy and Bradley, 1982; Shea,
1985). All specimens were dissected and assigned to one of the three categories based on sex and gonad maturity. Juveniles were defined as all individuals lacking visible gonadal development; at the juvenile stage it is impossible to determine sex by simple visual inspection of the gonads. However, sexes can be distinguished when gonads begin to mature, which occurred at slightly less than 50% of maximum adult size (20 mm standard length) in these samples.
Characters consisted of distance measures among 35 presumptive homologous landmarks (sensu Bookstein et a1., 1985; Fig. 2; Appendix). These landmarks provided endpoints for 42 "truss" distances (characters; Strauss and Bookstein, 1982). In this discussion, characters are identified by their endpoint landmarks. Measurements were taken both from lateral and dorsal projections. Some landmarks in the dorsal projection (Fig. 2, above) are equivalent points on the right and left sides of the fish. These are identified by the same number, 2 for example, with the left side identified as 2'. Bilateral characters, except for pectoral fin measures, were averaged and include such characters as 1-2 and 1-2',2-4 and 2'-4'.
Because pectoral fin rays are often damaged, the fin in better condition on each specimen was measured for characters 24-25, 26-27, and 28-29. Specimen projections were 20
...3 ··.4.
6
18
..... ~z1J~--=::~~~~~:,,:,,:,,:,,:,,:,,:,:,:,:,,:,:~~·o.· 3S
...... :.~.i .. :~: ...... / ...... • 0· • lyL ______~ ______~y3S
Figure 2. Mensurai characters measured in Paraclinus species. Open circles indicate presumptive landmarks used as endpoints for distance measures. Solid lines indicate distances (characters). 21 traced using a Wild dissecting microscope and camera lucida. This enlarged small distances and small specimens, reducing error in data collection. Landmarks identified on the drawings were then digitized and distances computed USing DIGITIZE and DISTANCE software (R. E.
Strauss).
Determination of General Size
Characters were logarithmically transformed to ensure homoscedasticity, linearize allometric effects, and standardize variances (Jolicoeur, 1963). Logarithmically transformed characters were analyzed using principal component analysis (PCA) of the covariance matrix.
The first principal component (PC1) of the within-species PCA was interpreted as a general size vector because the character coefficients were all positive and approximately of the same high magnitude (Bookstein et aI., 1985; Bookstein, 1989).
Sexual Dimorphism and Size
Sexual dimorphism may affect the score (size assignment) of an individual on PCl. If so, then size should be determined by monomorphic characters only, requiring an independent identification of dimorphic characters. Possible effects of sexual dimorphism on size assignment were investigated in one species, P. sini. Dimorphic characters were identified by analysis of covariance using standard length (snout to caudal edge of the hypural plate) as a proxy for body size; mature males and females were groups, standard length the covariate.
Individual specimen scores on PC1 of the full data set (monomorphic and dimorphic characters) were compared with their corresponding scores on PC1 of the reduced
(monomorphic) data set. Correlation of scores from the full data set with scores from the reduced data set was a highly significant 0.99, indicating that the two analyses do not differ in the assignment of body size scores. Because inclusion of sexually dimorphiC characters did not 22 alter the relative size assignments, use of the full data set in determining a general size vector for each species was justified.
Fitting the Models
Individual characters within species were fitted to all alternate models using Powell's direction-set algorithm, a general procedure for minimizing a function (the least-square deviations from the appropriate trajectory model in this case) that does not require specification of partial derivatives (Press et a!., 1986). For models having more than one spline in the regression (B and C) the direction-set algorithm was used to locate the divergence point for juvenile and adult trajectories. Because males and females are assumed to share the juvenile growth pattern, the regression of the diverging sex or sexes was constrained to intersect the juvenile trajectory for models Band C. Both these models were fit twice: first forcing this divergence point to occur between mean juvenile and mean female sizes (females were, on average, smaller than males) and second, allowing the divergence point to converge to the global optimum. Comparison of these constrained and unconstrained solutions allowed assessment of their relative stabilities. For many characters, the divergence point was identical for both the constrained and unconstrained solution, but for some (the three pectoral fin characters and one or two of the very small distances), the unconstrained optimum gave a divergence point at a size below zero or above the maximum size the species attained. In these cases there was too much variability in the data to assign a growth model with any confidence, in fact pectoral fin characters, 24-25, 26-27, and 28-29, proved to be too variable because of fin damage to assign to any particular model.
To determine which of the models provided the best fit for a given character, the regressions fit to models Band C were each evaluated for the improvement gained over models
A and B, respectively, using the following improvement-of-fit E-statistic (Neter and Wasserman, 23
1974:160-165):
E = [(SSEc- SSEr)/(df,- dfr))/MSEr , where SSEr is the error sum of squares for the full model, SSEr is the error sum of squares for the reduced model, MSEr is the mean squared error of the reduced model, and df, and dfr are degrees of freedom of the full and reduced models, respectively. "Full model" here refers to the model with fewer splines. Significance of improvement of fit was determined at f < 0.05, with (df, - dfr) and dfr degrees of freedom. When neither model B nor C provided a Significant improvement over model A, the character was considered to be monomorphic.
To compare character growth rates among the four species, character allometries for the four species were calculated using slopes given by the best fit model for each character.
Isometry in each species was determined as the mean slope of all non-dimorphic characters.
Allometric coefficients were scaled relative to this measure of isometry (Strauss and Bookstein,
1982).
To detect size-independent shape differences among males, females, and juveniles, three-group discriminate analyses were performed on residuals obtained by regresSing each character independently against the size vector. To avoid weighting problems associated with unbalanced design, sample sizes for males and females were equalized by randomly eliminating individuals from the data set.
RESULTS
Pattern of Dimorphism
The four species varied considerably in extent of shape dimorphism (Fig. 3). In the least dimorphic species, P. mexicanus, 4 of the 42 characters (9%) were dimorphiC. These include incision of the dorsal fin membrane (14-21, more continuous in males), and three midbody lengths (8-17, 7-17, and 8-16). The most dimorphic species was P. nigripinnis (55% 24 dimorphic); the other two species showed intermediate levels of dimorphism (36% and 38% for
P. sini and P. fasciatus, respectively).
Although the amount of dimorphism varies among species, the patterns of dimorphism tend to be similar (Fig. 3). In general, females have greater midbody and posterior-body lengths (characters 8-17, 7-17, 16-31, etc.). Combined, these increased lengths contribute to the longer female body at a given size (1-35, Figs. 2, 3) observed in three of the four species. In addition, females of all four species have a less continuous dorsal fin membrane between the third and fourth dorsal spines (14-21; Fig. 2), than do males. Other dimorphisms of the dorsal fin include the more elongate first dorsal spine (characters 7-18) of female P. fasciatus and P. sini and the spacing difference in dorsal spines (14-15) seen in P. sini and P. nigripinnis.
Males have longer and wider maxillaries (characters 1-10 and 9-11) than females in P. sini, P. nigripinnis, and P. fasciatus. A trend toward dimorphism in both jaw characters occurs in P. mexicanus, although statistical significance is marginal, at P = 0.055 for P. mexicanus as opposed to P < 0.001 for the other three species. Males of P. nigripinnis have both longer and wider heads than females (1-7, 1-6, 1-8,3-3'), while males of P. fasciatus and P. sini have shorter heads than females (1-7).
Pattern of Allometric Growth
In all four species, males, females, or both sexes diverge from juvenile growth trajectories with relatively equal frequency (Fig. 4, Table 1). For example,~. mexicanus has a total of six characters that fit model B or C significantly better than the null model, model A
Of these six characters, one best fits model B with males diverging (character 14-21), three best fit model B with females diverging (7-17, 8-16, 8-17), and two (2-4, 5-5') best fit model C (both sexes diverge). The two characters of P. mexicanus that follow model C growth are monomorphiC because adult allometries are equal, although both differ from juvenile allometry 25
P. mexican us
P. fasciatus
L------F--~------~
P. sini
M 1
P. nigripinnis MM 't,"
Figure 3. Dimorphism patterns for 4 Paraclinus species. M = dimorphic, male larger; F = dimorphic, female larger, unlabeled lines indicate monomorphic characters. 26
Table 1. Summary of the divergence pattern for Paraclinus species. Values indicate the number of characters that best fit each model.
Species Model A Model B Model C
Mooomotpbi< Dimotpbic Either Moao- or MII.Di~ Femll. Di""'B"l' Equivocsl Dimotpbi< P. me:cicanus 33 3 0 2 P. [asciatus 21 10 6 0 2 P. sini 19 6 7 6 P. nigripinnis 12 11 6 3 7 27
(Fig. 1, model C, right). This is not necessarily the case with other species which show model
C type growth. For example, in P. nigripinnis, allometric coefficients for character 1-8 (head
depth), which fits model C, are 0.75, 1.00, and 1.21 for juveniles, females, and males
respectively, and this character is clearly dimorphic.
Size-Independent Shape Differences
Discriminate analyses (Fig. 5) of shape residuals show that in each species, males and
juveniles are more similar to each other than either is to females, as evidenced by their
proximity in the shape space described by the two discriminate axes. The first axis accounts for
more than 97% of the among-group variation in each species. The characters which contribute
to group separation (those that correlate significantly with this axis) are almost exclusively
dimorphic (Table 2).
DISCUSSION
The assumption that differential growth in males is the sole ontogenetic cause of sexual dimorphism in adults is not upheld by these results, rather, dimorphism is produced by allometric changes occurring in both sexes with approximately equal frequency. The roots of
this divergent male assumption probably lie in the most common hypotheses for the evolution
of sexual dimorphism. Sexual dimorphism has been attributed to selection in one of three
general categories: sexual selection (Darwin, 1871; Campbell, 1972), selection for ecological
divergence (Darwin, 1871; Selander, 1966; Shine, 1989), and selection for optimal fecundity
(Darwin, 1871; Lindsey, 1975; Shine, 1989). Historically, the latter two categories have been
largely neglected in favor of the first (Cooper and Vitt, 1989; Slatkin, 1984; Shine, 1989), and
sexual selection theory in general attempts to explain male and female differences in terms of
male change in morphology. This implicit assumption of the male as the 28
P. mexicanus
P. fasciatus
P. sini :~/\=::::::::::~ F B~~ B
~------M------~
Figure 4. Divergence patterns for 4 Paraclinus species. Lines labeled M = model B, males diverging, F = model B females diverging, ? = model B, equivocal; B = model C (both sexes diverge); unlabeled lines = model A growth. 29
F n = 11
DF2 DF2
2.3% 1.3%
n = 16 n = 15 n = 16 Paraclinus mexicanus n = 15 Paraclinus fasciatus
OF1 97.7% OF1 98.7%
D n = 16 n = 16 OF2 n = 11 DF2
0.1% 0.9% n = 16 n = 16 \) n = 13 Paraclinus nigripinnis 0 Paraclinus sini
OF1 99.9% OF1 99.1%
Figure 5. Plots of relative group positions from size-free discriminate analysis. DFI = first discriminate function, DF2 = second discriminate function. The amount of among-group variation accounted for by each function is represented along each axis as a percentage. Polygons enclose individuals within each group: M = males, F = females, J = juveniles. 30
Table 2. Character correlations with the fxrst discriminant function, OFl. Negatively correlated characters are relatively larger in males, positively correlated characters are relatively larger in females. D = sexually dimorphic character as determined by fit to model B or C, significance level indicated by • or •• (P < 0.05 or P < 0.01, respectively).
Body Character P. sini P. mexicanus P. fasciatus P. nigripinnis Region
Head 1-7 0.48**0 0.05 0.45**0 -0.40**0 1-8 -0.22 -0.05 -0.12 -0.67**0 1-6 0.18 ------. -0.50**0 7-6 ---- -0.24 -0.280 0.11 12-6 0.16 -0.28 -0.22 0.35*0
7-8 -0.09 ---- 0.34* 0.17 1-2 0.15 -0.14 -0.03 -0.240 2-4 -0.25 -0.07 -0.05 -0.77**0 4-5 0.47**0 0.18 0.30*D 0.53**0 5-5' -0.15 -0.10 0.12 0.33*0
4-4' -0.13 0.18 0.21 ---- 3-3' -0.30* 0.13 -0.080 -0.66**0 2-2' -0.40** -0.42** -0.21 -0.25
Midbody 7-12 -0.32* -0.08 0.29 -0.08 12-13 -0.11 0.11 0.14 0.27 13-14 0.13 0.19 0.23 0.16 14-15 0.49**0 -0.10 0.27 0.46**0 15-16 0.42**0 0.18 0.65**0 0.53**0 8-17 0.72**0 0.46**0 0.76**0 0.63**0 7-17 0.62**0 0.54**D 0.75**0 0.65**0 8-16 0.74**0 0.35*0 0.77**0 0.75**0 16-17 0.07 ---- 0.45**0 0.75**0
Posterior 16-30 0.19 0.22 0.32*0 0.50**0 30-31 0.13 -0.17 ---- 0.20 31-32 -0.07 -0.21 0.24 0.25 32-17 -0.12 ---- 0.19 -0.06 31
Posterior 16-31 0.26 --- 0.40**0 0.56**D 17-30 -0.16 --- 0.22 0.24
Jaw 1-10 -0.61**0 -0.46" -0.72**0 -O.86**D 9-11 -0.74**0 -0.29 -0.70**0 -O.71**D
Median fins 7-18 0.44"0 0.15 0.14D 0.28 12-19 0.35**0 0.22 0.14 0.14 13-20 -0.07 0.17 -0.12 -0.10 14-22 om -0.02 -- 0.26 14-21 -0.79**0 -0.38*D -0.82**0 -0.33*D 15-23 -0.05 0.30* -- -- 32-33 0.12 0.00 0.12 -0.10 17-34 -0.23 0.08 0.33*D -0.40**D
Length 1-35 0.47 **0 0.32* 0.66**0 0.42**D 32 evolutionarily divergent sex is then carried over into an assumption of the male as the ontogenetically divergent sex.
In the four species studied here, even characters such as wider male head size that might give advantage in aggressive male interactions and thus may be under selection for larger size in males were not predictably formed by male ontogenetic divergence. In P. fasciatus, for example, the wider male head (character 3-3', Figs. 2-4) results from a decrease in female allometry relative to a common juvenile-male allometry (Fig. I, model B female diverging).
Allometric coefficients are 1.24 for juveniles and males, 0.15 for females. Conversely, in P. nigripinnis, the wider male head results from an increase in both male and female allometries compared to the juvenile, with a relatively larger change in the male allometry (Fig. 1, model
C, dimorphic growth). The allometric coefficients for this character are 1.16, 1.37, and 0.8 for females, males, and juveniles, respectively. Likewise, larger midbody of the females, generally explained as an adaptation for greater egg-bearing capacity (Lindsey, 1975), is sometimes a result of slower growth in males rather than acceleration of growth in females. For example, in
P. fasciatus the larger midbody of the females (15-16,7-17,8-17,8-16) is entirely due to slowed male growth (Figs. 3, 4).
These examples illustrate that a particular hypotheses for the evolutionary origin of sexual dimorphism in not sufficient to predict the growth pattern leading to that dimorphism.
Likewise, the observed allometric changes during ontogeny may not exclude a particular evolutionary hypothesis, since ontogenetic change does not necessarily imply phylogenetic change. Evolutionary allometric change (and thus the origin of dimorphism) should be evaluated relative to an outgroup allometry (Fink, 1982). Confusion of ontogenetic divergence with evolutionary divergence may cause unwarranted explicit or implicit characterization of juvenile or female allometries as representative of the ancestral condition (e.g., Cheverud and
Richtsmeier, 1986). An understanding of the ontogenetic origins of sexual dimorphism, 33
coupled with hypotheses of the probable ancestral trajectories, should help distinguish among
general hypotheses concerning the evolutionary origin of dimorphism.
At least in fishes, the general view of males as the divergent sex: may partially result
from a greater resemblance between juveniles and females than juveniles and males. However,
resemblance of females to juveniles can be misleading in that similarity of female shape to
juvenile shape may be produced by a slowing of growth in females relative to juveniles and
males rather than by female and juvenile allometric Similarity. For example, the juvenile
condition of a dorsal fin incision (14-21) is also present to some extent in females of all four
species. In female P. sini and P. fasciatus, growth of the dorsal fin membrane slows, resUlting
in a very distinct notch in the female dorsal fin, a condition which resembles that of juveniles.
Males of these species follow the juvenile trajectory of increased membrane growth up the
dorsal spine, eventually resulting in a continuous dorsal fin membrane. The oppOsite is true in
P. mexicanus. Thus, the presence of such juvenile-appearing morphology in adult females may
be a result of allometric change in either sex.
In view of the generalization of female and juvenile resemblance, the results of the
discriminate analysis revealing females as more different in shape (when size and allometry are
accounted for) from juveniles than males were somewhat surprising. The closer placement of
juveniles and males in morphospace (Fig. 5) indicates that, overall, female shape diverges
relatively more from juvenile shape than does male shape. Dimorphic characters account for
most of the group discrimination, as shown by their correlations with the first discriminate axis
(Table 2). This trend is not explained simply by number of female-divergent versus male
divergent dimorphic characters. In P. mexicanus and P. sini, female-divergent characters slightly
outnumber male-divergent characters, while for P. fasciatus and P. nigripinnis, male-divergent
characters outnumber female-divergent characters, yet in all species juvenile shape is more
similar to male than to female shape. When male-divergent characters outnumber female 34 characters, female allometries must change relatively more for female divergence to produce this pattern. At least for these fishes, females are not shaped like large juveniles. The perception of females as having juvenile appearance probably results from observing and emphasizing one or two paedomorphic characters while overlooking the many more subtle differences between females and juveniles, including those that this analysis has uncovered.
The type of growth leading to a particular dimorphism may also be compared among species to evaluate homology of dimorphism. When the similar adult morphologies among species result from different growth patterns, as in head width discussed earlier, homoplasy is implied. Several characters show a pattern in which dimorphic similarity among adults of two or more species originates in very different ways during growth. In addition to head width
(character 3-3') several other characters follow this pattern. For example character 4-5, an element of head length (Fig. 2). is larger in females than males of both P. sini and P. !asciarus
(Fig. 3). but the sexes diverge by increased growth in females of P. !asciatus while in P. sini, males decrease growth for the same overall effect (Fig. 4). In several other characters (14-21.
8-16, 7-17) similar dimorphism among the adults of two or more species resulted from dramatically different growth patterns. These differences in growth indicate that the adult conditions of these characters are not identical as ontogenetic characters, and therefore are not homologous, although examination of only adult specimens might lead to the oppOSite conclusion.
CONCLUSIONS
Sexual dimorphism in Paraclinus is not produced simply by allometric shifts in male growth.
Rather. changes in allometry of both sexes produce the shape dimorphism seen in adults. In addition, elaboration of a trait in one sex does not reliably indicate that this sex is the one in which growth rates diverge from those of the juvenile. The assumption that males are 35 ontogenetically divergent for those characters which seem elaborated in males focuses hypotheses for the evolution of such dimorphism on male interactions and on sexual selection in general, drawing attention from equally important changes in female and juvenile growth and form. Female shape is not the standard against which change in male shape should be measured. Knowledge of how changing allometriC growth gradients produce sexual dimorphism within species, ideally coupled with a phylogenetic hypothesis, will allow better directed hypotheses for the evolution of sexual dimorphism. 36 CHAPTER TWO
PHYLOGENETIC RELATIONSHIPS OF THE TRIBE PARACLININI
ABSTRAcr Phylogenetic relationships have remained unresolved for labrisomid blennies of the tribe ParacIinini, though the taxa themselves are well known. Using parsimony analysis and a combination of osteologic and morphologic characters, I examine the relationships within this group. Cladistic analysis allowed identification of three main paraclinin lineages. The species pair, Paraclinus integripinnis and P. walkeri forins one such lineage. Sister species P. beebei and P. fehlmanni plus their outgroup, P. tanygnathus form another, the last is comprised of five species; P. infrons as sister species to the monotypic genus Exerpes, with P. barbarus, P. mamzorarus, and P. naeorhegnzis as their successive outgroups. Paraclinus grandicomis seems to be the most primitive member of the clade. Beyond identifying these lineages and the most primitive members, relationships remain largely unresolved. The pOSition of Exerpes in the phylogeny indicates that its single species should be included in Paraclinus. INTRODUcrION The labrisomid blenny tribe Paraclinini is comprised of two genera, Exerpes Jordan and Evermann and Paraclinus Mocqard, containing one and twenty nominal species, respectively. These small marine fishes are restricted in distribution to the American tropiCS, with eight occurring in the western Atlantic Ocean and thirteen in the eastern Pacific Ocean. When Hubbs (1952) first erected the tribe, he also included within it the genus Auchenistius Evermann and Marsh as well as Paraclinus and Exerpes. Hubbs characterized the 37 Paraclinini as having a spine on the opercle, a reduced number of dorsal soft rays (0-2), large lateral line scales, and few cirri. Springer (1955) subsequently synonomized Auchenistius with Stathmonotus Bean, but retained it within the Paraclinini based on reduced number of dorsal rays. He found, however, no opercular spine on most specimens. Recent work by Hastings (pers. comm.) indicates that Stathmonotus is unrelated to Paraclinini, which leaves Ererpes and Paraclinus as the sole members of the tribe. The presence of an opercular spine and reduced number of dorsal rays support the monophyly of the two genera. Although all known paraclinin species have been described, little progress has been made in determining relationships among them. Hubbs (1952), Springer (1955), Bohlke (1960), Springer and Trist (1969), and Rosenblatt and Parr (1969) all discuss relationships only to the extent of identifying groups of 1 to 4 species that seem to be closely allied. All were unable to place subgroups into any larger phyletic context. The purpose of this study was to examine paraclinin relationships in a phylogenetic context using osteological data that had not been previously considered for within-group relationships as well as computer programs and methodology that have become available since previous researchers last turned their attention to this group. MATERIALS AND METHODS Taxa examined: Outgroups and polarity assessment Relationships among the blennioids have been problematic at best for quite some time (Hubbs, 1952; Springer 1955, 1966, 1968; Stephens 1963; Springer and Smith-Vaniz, 1972; Bohlke & Springer 1975; George & Springer, 1980). Currently there are six recognized families of Blennioid fishes, Blenniidae, Dactyloscopidae, Trypterygiidae, Clinidae, Chaenopsidae, and Labrisomidae (Nelson, 1984). Labrisomidae currently contains six tribes; Paraclinini, Neoclinini, Cryptotremini, Mnierpini, Labrisomini, and Starksiini. This family, 38 however, lacks any synapomorphies supporting its monopyly. It seems likely that the closest relatives of some labrisomid blennies are contained in other families (Hastings, pers com). In addition, not all species fit easily in one of the recognized tnoes, showing affinities with several depending on which characters are emphasized (Bohlke & Springer 1975). This makes choice of an outgroup to the Paraclinini problematic at best. Rosenblatt & Taylor (1971) felt that the presence of fewer than 2 pterygiophores anterior to the first haemal spine in female Starksia and Exerpes suggests kinShip between the tribes Paraclinini and Starksiini. This condition is also seen in all Paraclinus examined (Figure 6) but is not present in the other Starksiin genus, Xenomedea. Stepien (1992) analyzed DNA sequence and allozyme data for selected blennioids. Although the DNA data set was not relevant to the relationships here, the allozyme analysis included all six labrisomid tribes as well as two of the three clinid tribes. Her analysis suggests that Labrisomidae is indeed paraphyletic, with Clinidae as a sister taxon to the labrisomid tribe Cryptotremini. Her most parsimonious tree shows Paraclinini and Starksiini as sister taxa (Figure 7A), with Cryptotremini as sister taxon to the family Clinidae. The Labrisomini and Mnierpini are sister taxa on the next node down. However, with just one more step, two alternate trees are obtained (Fig. 7B), so the sister relationship of Paraclinini and Starksiini is uncertain. In the face of this lack of resolution, I chose to collect data from representatives of both starksiin genera, Xenomedea and Starksia, one cryptotremin, Alloclinus holden, two labrisomins, Labrisomus phillipi and Malacoctenus hubbsi, and one clinid, Gibbonsia elegans. I also constructed a hypothetical outgroup by comparing character states among the possible outgroups (Hastings, 1990). When possible outgroup taxa agreed for a character state, the hypothetical outgroup was asSigned that character state. When there was conflict, the state was listed as unknown. Phylogenetic analyses were run with all outgroup genera simultaneously, singly, and in various combinations to see how their inclusion and order affected topology of 39 Paraclinus integripinnis Exerpes asper Xenomedea rhodopygia Starksia spinipenis Figure 6. Anterior anal pterygiophore arrangement in Paraclinini and Starksiini. 40 I j i J. i -: i j I I E i ! i I t t i ! f . ! I 1I ! : 1 ill i i=i i jjl! tf ! ....i ·.; .: .i !f! J t i.· i ~~· i. .a· : 1I ...i .. =i : ! :E : 1 •II l j j •' ..I ...=. t • • • • ..• J -: : I f' • • I "' ~- ...... '.' ! •• i J -;••••• -; .: .. .. ~f/ i I i ~ f IT ~ i f ,l f I 1i ~ l ! ! i i _Par.. llnlnl ltarkellnl Laltrlaor~~lnl Mnlorplnl Nooollnlnl Cllnlnl M1•9dlnl I Ic,.,ptotror~~tnr I I I l A Labrleor~~ldaa/CIInhl .. ------~----~ --=a -a ~ -~ •... -=a - J:1 ., -...... J:1 a -~ - -0 - -=a 0 p...... -~ ~ ...-• 0 • -... - ... - ... 0 -~ ~ •... -.a • -0 ... ~• ~ -u u ., p..• ..:I • - • - ~ I I =- ' B Figure 7. Relationships among five blennioid families based on allozyme data. Figure follows Stepien (1992). Dotted line on the lower diagram indicates alternate affiliations among Starksiini, Paraclinini and Cryptotremini. 41 the ingroup. Ingroup taxa All twenty-one known Paraclinin species were examined for this analysis: twenty Paraclinus and the one species of the monotypic genus £Xerpes. Table 3 lists the species names, the number of alcohol-preserved specimens examined, the number of cleared and stained specimens examined, and the source (museum and lot number) of the specimens. Alcohol preserved material was examined for all ingroup species and for the five outgroup taxa. Cleared and stained specimens were examined for all but three rare taxa, P. ditrichus, P. magdaienae, and P. stephensi; these were unavailable. These species were necessarily scored as unknowns for all osteological characters. Since I often had only one cleared and stained representative of each species, I used P. sini as an indicator of possible variability for osteological characters. For example, the number of pro current rays in the caudal fin might be a useful character. These vary between 3 and 5 rays within Paraclinini and 5-9 rays in the outgroups. Within P. sini the rays vary from 3 (9 of 10 specimens) to 4 (1 specimen). While there is likely phylogenetic information in the modal number of procurrent rays, it would be necessary to collect data from many specimens within each species in order to assign character state correctly. Many characters like this could provide phylogenetic information if larger sample sizes per species were available, allowing statistical analysis of within and among species variability. Characters The 40 morphological characters used for the analysis include osteological, head pore/canal and soft body. Table 4 lists characters, numbers, and state asSignments. Reference to all characters will foIlow the numbering system represented there. Non-informative characters (autapomorphies of one taxon) were excluded from the analysis. Of the 40 characters used, 34 were binary and 6 were multistate. Three of the 42 Table 3. Material examined for phylogenetic analysis. Institution abbreviations as follows: SIO = Scripps Institution of Oceanography; USNM = United States National Museum of Natural History; ANSP = Academy of Natural Sciences of Philadelphia; CAS = California Academy of Sciences; LACM = Natural History Museum of Los Angeles County; UF = Florida Museum of Natural History; UA = University of Arizona; UACS = University of Arizona (cleared/stained); MB = Meriel Brooks colI. # alch = number in alchohol; #C/S = number of cleared and stained specimens examined. Species ## Source ## Source alch CIS Paraclinus 13 SIO 66592; 6791 2 USNM 199063 grandicomis USNM 197654; 199063; 297473 SI06791 A.l\ZSP 75232; 111674; 124699 P. barbatus 23 fM1Ii"H 90301; 90300; 90299; 96777; I FMNH96717 96792;96771;94401; 7018S;87839; 87840;87841;87843;94018;94019; 96717;96789 US!I.'M 267819 P. cingulatus 49 n1~"H 84480; 90302: 90303; 90304 2 FMNH90302 US!I.~1 163275; 306528 US!,;"M 306528 A..'';SP 98909; 72312: 94612: 94613: 94615;98910;92609;92608: 103006; 145876; 113213: 72311: 92607 P. fasciatus 156 SIO 6787: A."'ISP 143486: 093972 1 ANSP 14386 P. infrons 48 FMNH 90311; 96750; 96863; 94402; 3 FMNH96750 96782;96772;89359;96820;96788; ANSP 121436 96747: 94303: 87844: 96718; 90310; U~1267821 90309:93859;94119:87845 VSNM 267821: 308396 A.l\ZSP 121437; 121436 lJr 13940 P. marmoratus 134 CAS 66906; 66907: 66908; 66909; 1 CAS66906 66910: 66911; 66912 USNM 176247; 134304; 297512 UF 11840; 18939; 24364; 2S339; 25863 P. nigripinnis 81 SIO 6787 1 ANSP94623 A..-';SP 094618; 094623; 143116 P. naeorhegmis 10 ANSP 094617; 92982; 92984; 94616; 1 ANSP 94617 115116 P. sini 167 VA 7138 9 MBCS 4. 3 6 VA 6873, 7350 P. beebe; 161 S106225; 6256; 620706; 6255: 62241 4 VA 6837: 6838 S10625551 43 P. mexican us 151 VA 694822 3 VA 69422 P. ditrichus 3 SIO 62861: 61250 0 P. integripinnis 229 SIO H5134; 70149; 70271: 58481 5 VA 73762 MBCS 12 P. walkeri 164 SIO 60455:60457: 69384 2 SIO 69384 P. tanygnathus 17 LACM 9045-3; 9051-35 2 SI023961 SIO 61-239: 62-8; 65-186; 70-158; 70- 165 P. altivelis 27 SIO 65-329; 65-299 2 S106532961 P. magdalenae 7 SIO 64-61: 64-45: 64-43 0 P. stephensi 2 SIO 62-25 0 LACM 9044-2 P. monophthalmus 73 VA 68-76: 68-77 3 VA 68781 SIO 71-3: 71-253 P. /ehlmanni 28 VA 68-56: 68-58 3 VA 685820 SIO 74-66 Exerpes asper 63 MB 052187-1; 52687-1; 52787-1; 9 MBCS 8. 9,10,11 52787-2: 52887-1: 60487-1 VA85-4 Slarksia spinipenis 3 VA 67-66 4 VA 7525 S. y-lineata 0 1 VF 10736 33 UF 67-66 S.ocellala Xenomedea rhodopyga 21 UA 67-90 7 VA 7214; VA 71211 Alloclinus holderi 0 1 NolO .\1alacoctenus hubbsi 0 5 VACS 41. 42; MBCS 1 VA 68758 M. zoniJer 0 1 7 5 VACS 40 .\1. gigas VA 69-38 Gibbonsia elegans 2 MB-2 2 MBCS2 Labrisomus phillipi 2 t;A 68-53 1 VA 685212 L. mulliporosus 2 VA 68-55 0 44 Table 4. Characters and character states used in phylogenetic analysis. # Description Ord States ered ? 1 Last dorsal elements yes 0=>2 soft rays 1 = 1-2 soft rays 3 = 0 soft rays 2 Pterygiophores 1 and 2 yes o = rear of skull 1 = midskull 2 = anterior skull 3 PteI}"giophore 3 yes o = between Newal spines 3-4 1 = NS 2-3 2 = NSI-2 3 = anterior to NS 1 4 Third pelvic ray no 0= present 1 = rudimentary 5 Opercular spine no 0= absent 1 = present 6 Opercular spine stoutness no 0= weak 1 = strong 7 Opercular spine shape no 0= flat 1 = conical 8 Neural spine on flrst preural no 0= absent vertebra 1 = present 9 Number of elongate pre-caudal no 0=2 neural spines 1 = 1 10 Preopercular pores no 0= paired 1 = unpaired 11 Infraorbital pores no 0= paired 1 = unpaired 12 Supratemporal commisural pore no o = elaborate, lateral pores (PI) 1 = reduced or absent 13 Supratemporal commisural pore no o = elaborate, lateral pores (P2) 1 = reduced 14 Supraorbital commisure: no o = with 3 pores posterior I = with 5 pores 15 Lateral supraorbital pores no 0=4 or more 1=3 or fewer 45 Table 4. Continued 16 Frontal, series 1 no o = pore on tube 1 = tube with 2-3 lateral pores 17 Frontal, series 2 no o = pore on tube or canal 1 = absent 2 = tube with lateral pores 18 Lateral line no o = continuous 1 = interrupted 19 First dorsal spine no 0= thick 1 = extremely thin 20 Second dorsal spine no 0= thick 1 = extremely thin 21 Pelvic girdle no o = open ventrally 1 = closed ventrally 22 Pelvic threads no 0= present 1 = absent 23 Bony sheet above opercular no o = half or less spine length spine 1 = entire spine length 24 Lateral process on no o = simple point or ridge hyomandibular I = point with av ridge or process 25 Pectoral fm rays no 0= 13 or more 1 = 12 26 Ventral postcleitbrum shape no 0= spur 1 = flange or point 27 Anal fm membrane attachment no o = anterior of caudal fm 1 = on caudai fm 28 Anal fm membrane attachment no o = half or less ray length on last anal ray 1 = most of ray length 29 Shape of suborbital 2 no 0= short 1 = long 30 Shape of suborbital 3 no 0= long 1 = short 31 Scalation of pectoral base and no o = well scaled nape 1 = bald 46 Table 4. Continued 32 Nape cirri no 0= complex 1 = simple 33 Nostril cirri no 0= complex 1 = simple 34 Dorsal fm membrane no o = continuous 1 = incised 35 Basisphenoid no o = small, at rear or orbit 1 = extends halfway into orbit 36 Pterosphenoid no o = without anterior projections 1 = with anterior projections 37 Dorsal spines 1 and 2 no 0= <=DS9 1 = >DS9 38 Dorsal spine 3 no 0= <=DS9 1 = > DS9 39 Dorsal spine 4 no o = > 0.6x length of DS9 1 = < 0.6x length of DS9 40 Maxilla length no o = extends halfway to rear of orbit 1 = extends to anterior of orbit 2 = exteds beyond rear of orbit 47 multistate characters were ordered: #1, the reduction of dorsal rays from more than 8 to 1 or 2 (which partially defines the Paraclinini) and from 1 or 2 to 0 (variable within Paraclinini); #2, the position of dorsal pterygiophores 1 and 2 relative to the skull and first neural spine; and #3, the position of the third pterygiophore relative to the vertebral column and skull. Figure 8 shows the possible states for these two characters. Ordering characters #2 and #3 assumes that the first three pterygiophores and their spines shift anteriorly or posteriorly in increments, rather than changing from one extreme position to another along lineages. Homology of the first three spines is supported by the fact that in all paraclinins and the outgroups examined, the 4th dorsal pterygiophore always lies between neural spines 4 and 5, and is at least positionally homologous among groups (Figure 8). If spine and pterygiophore losses were causing apparent positional differences between dorsal pterygiophores with their associated spines, I would expect the number of spines and/or pterygiophores anterior to the 5th vertebra to vary, which does not occur in the groups considered here (there are always 4). It is interesting that in Stathmonotus the anteriorrnost pterygiophore lies in front of the 3rd neural spine, suggesting that the rear position of the dorsal fin result from loss of the first two dorsal spines rather than a posterior migration of the first dorsal spine. Character states present in the various outgroups are depicted in Figure 9. Anterior dorsal spine proportions themselves vary tremendously within the clade, particularly the first five or six. This results in dorsal fin outlines varying from a rather low even dorsal fin to a triangular shaped fin (Figure 10). Characters #37-39 describe the height of the first three dorsal spines relative to the height of the ninth, which was taken as an average spine size. Anterior spines also vary in thickness. Fin spines in this group are very stout as a rule, but in some species the first three spines are quite thin and flexible. I measured spine thickness and defined the character state "extremely thin" as anterior spines with less than half the average width for randomly chosen posterior spines. The first two 48 Paraclinus grandicomis Paraclinus walkeri #2 state = 1 #2 state = 0 #3 state = 1 #3 state = 1 Paraclinus infrons Paraclinus barbatus #2 state = 2 #2 state = 2 #3 state = 2 #3 state = 3 Figure 8. Illustration of character states for #2 and #3, the position of the first three dorsal pterygiophores in relation to the skull and anterior vertebrae. 49 AlloclillUS holderi Labrisomus phillipi Xenomedea rhodopygia Gibbonsia elegans Figure 9. Characters #2 and #3 as seen in possible outgroups of Paraclinini. ----_.------50 Paraclinus nigripinnis - Paraclinus mannoratus Figure to. Low square dorsal fin illustrated by nigripinnis, high triangular dorsal fin illustrated by nzamlOratus. 51 dorsal spines always share the same state and were coded as one character (#19). The caudal skeleton provided a few characters, although there was enough variation within some species to cause me to delete many from the initial data set. For example, there seems to be some useful variation in caudal cartilages, but I was unable to ~e these as my sample sizes were too small. Cartilage stains so variably that a large sample is necessary to confirm absence of a caudal cartilage. The two characters which seemed constant enough to use were #8, the presence of a neural spine on the first preural vertebra and #9, the number of elongate neural spines associated with the caudal fin (Figure 11). The pelvic fins and girdle provide three characters, #4, #21, and #22. The number of pelvic fin rays is primitively 3 in the blennioids. Within paraclinins, the third ray varies from somewhat reduced in size to absent except for a vestigial ossification at the base of the fin (Figure 12a). This vestige can be seen only on cleared and stained specimens. The pelvic girdle itself varies from being long and tubular with the ventral edge closed to more rounded with the ventral edge open (Figure 12b). From the dorso-posterior end where the two basipterygia fuse, there are two elongate ossifications extending in a ventro-anterior direction (Figure 12b). These have become reduced or lost within Paraclinins. Hastings (1990) found a parallel change among species tube blennies of the genus Acanthemblemaria. The opercular spine, which defines the group, varies within the group as well (#5-#7). In some species the spine is very stout and considerably reinforced, while it is relatively thin and weak in others (Figure 13a,b). It also may be fiat, with a rounded to multifurcate posterior edge, or sharp and conical. Dorsal to the opercular spine is a sheet of bone that may extend posteriorly to the end of the spine or truncate less than halfway along the spine (character #23, Figure Bc). Because none of the outgroups have an opercular spine, they were scored as unknown for these characters. All the Paraclinini, with the exception of Exerpes, have 4 suborbital bones. Exerpes has 52 Figure 11. Characters #8 and #9 illustrated by walkeri (above) and monophthalmus (below). Presence or absence of a neural spine on the first pre-ural vertebra, and the number of elongate neural spines associated with the caudal structure. 53 A B Figure 12 Vestigial third pelvic ray in jasciarus (A). Pelvic threads with open pelvic girdle in Labrisomus phillipi. 54 P. monophthalmus weak flat opercular spine entire bony sheet (above o. spine) P. mamloratus strong conical spine B truncated bony sheet c P. nigripinnis strong flat spine truncated bony sheet Figure 13. Possible conditions of the opercular spine in paracJinin blennies. 55 lost suborbitals 2 and 3, a condition probably associated with the extreme elongation of the snout. In the rest of the tribe, all four suborbitals vary in shape and orientation. For example, in some species the lachrymal is more forward in position, extending to just below the anterior 1/3 of the orbit, while in others it is positioned more ventrally and extends funher back (Figure 14a). In addition, some species have long tubular suborbitals while in others they are all shoner and broader (Figure 14b). I quantified the shapes of all four suborbitals by measuring their lengths and widths for each species. These measures were then plotted to see whether they fell out into any discontinuous groupings that could be coded as separate character states. Only two, the shape of S02 and S03, showed such discontinuity and could be used as discrete characters (#29 #30). The lachrymal and founh suborbital show no such clustering. They vary continuously and any subdivision into character states would have been completely arbitrary. The neurocranium of the Paraclinini shows little discontinuous variation, although there is much continuous variability in bones due to head shapes varying from more rounded to extremely long and pointed. The basisphenoid (#35) may be small and be confined to the rear of the orbit, or be quite large and extend anteriorly to the middle of the orbit (Figure 15a). The pterosphenoid (#36) sometimes has anterior projections that extend into the orbit and may fuse with the basisphenoid (Figure 15b). Pectoral fins and girdle are fairly conservative within the tribe. The ventral postcleithrum (#26) does vary in shape ending ventrally in a point or flange in some species or in a well developed anterior spur in others (Figure 15c). One interesting character of the suspensorium is a lateral process on the hyomandibular (#24). This process occurs at the juncture of the hyomandibular and the preopercular and usually has some sort of dorso-posterior projection (Figure 16a,b), such as a point or simple ridge very similar to that described for Nemaclinus atelestos by Bohlke and ------56 A. Paraclinus grandicomis B. Paraclinus sini c. Paraclinus altivelis D. Paraclinus infrons E. Exerpes asper Figure 14. Various shapes of the suborbital bones in Paraclinini. Note that Exerpes is missing suborbitals 2 and 3. 57 - -- A t B ~------ c Flange Point Spur Figure 15. Alternate character states of the basisphenoid (A), pterosphenoid (B), and ventral posl-cleithrum (C). 58 Springer (1975). Another ridge may extend ventro-.anteriorly, providing an anchor for a ligament running to the posterodorsal process of the articular (Figure 16c,d). Previously, the anterior process was described only in Starksia and Xenomedea, but the same condition is present in Paraclinus fehlmanni (Figure 16d). Length of the maxillary bone (#40) was included even though this character is dimorphic in many species. Although it is generally longer in males than in females of the same species, proportional differences are maintained among species such that when males have a very exaggerated maxillae, females of that species have a longer maxillae as well. Three states were defined: the maxilla may end in the anterior half of the orbit, extend to the rear of the orbit, or extend far beyond the rear of the orbit, almost to the preopercular bone (Figure 17). I described 9 sensory pore characters that are variable among the Paraclinins. Rather than focus on counting numbers of pores, I tried to identify the main pores and the underlying canals with which they were associated in a qualitative way. I follow Fukao (1987) for terminology of the two posterior extensions of the supraorbital canal. Figure 18 shows the various canal systems as well as the terminology and abbreviations used. Within Paraclinini, there are generally 6-8 preopercular pores, which may be paired or unpaired (#10). These lead into the mandibular series ventrally, which are not variable within the clade. Preopercular and infraorbital (#11) pores were scored simply as paired or unpaired. The postotic canal usually has two dorsal pores and one ventral pore. These are variable within species and were not used as a character. The otic canal has occasionally 2-3 pores, sometimes none. There are no very large pores that occur consistently, so I did not attempt to use these as a character. The supratemporal commissure has the basic configuration shown in Figure 19. There is generally a median commissural pore, which may be paired. On each side, there are two 59 \ \.~\ I \~ /}-- B c D Figure 16. Various conditions of the lateral process on the hyomandibular. A = simple point (Jasciarus). B = simple ridge (monophthalmus). C = point with ridge (walkeri). D = point with anterio·ventral process (Jehlnzanni). 60 A. Paraclinus gralldicomis fl o B. Paraclinus naeorhegmis c. Exerpes asper Figure 17. Variation in maxilla length within ParacIinini. 61 __J.~~r--- - Figure 18. Terminology used in identifying head pores with underlying canal systems. SO = supraorbital; a = otic; PO = post-otic; POP = preopercular; 10 = infraorbital; STC = supratemporal commisure; MD = mandibular; F1 = frontal, series 1; F2 = frontal, series 2; STCP1 & STCP2 = supratemporal commisural 1 and 2; SOC = supraorbital commisure; N = nasals. 62 dorsal extensions of the canal which I call supratemporal commissural pores 1 and 2 (#12, #13; STCPl and STCP2). Each may be a pore on the canal, a pore on a dorsally extended tube, or have a number of lateral pores on the tube. The nape cirri, when present, always lie between these two pore systems along the canal and are situated above a pore which opens posteriorly. There are similar anterior extensions of the supratemporal canal, but because they seem to be more variable I excluded them from this analysis. The supraorbital canals have 1-4 main pore openings laterally (#15), and usually two branches medially which extend dorsally and medially to the center of the neurocranium as frontal series 1 and frontal series 2 (#16, #17; F1, F2 in Figure 19). There are a variable number of smaller associated medial and lateral pores of the supraorbitals. The supraorbital commissure (#14) has one median posterior pore and generally one lateral posterior pair (Figure 19). There may be an additional pair at the junction of the supraorbital canal and commissure. Because of its placement it is difficult to tell which of these canals it is primarily associated with, so I placed it with the commissural series (SOCP2). Two species have the median commissural pore posteriorly extended on the tube (Figure 19). At the junction of the frontals and nasals, parac1inins always bear one lateral pore that lies just dorsal to the posterior nostril (Figure 19). In some individuals this is paired with a medial pore, in others it is not. The nasals themselves always bear at least two pores, located on the lateral edge of the canal. One is just anterior to the posterior nostril, the other is at the anterior end of the nasal bone (N1 and N2, Figures 18, 19). Again, these may be paired medially or not. Nasal characters were not used in this analysis because of within species variability. Other characters included condition of the lateral line (#18), whether the anterior dorsal fin membrane (#34), and the attachment of the dorsal and anal fin membranes to the caudal fin or caudal peduncle (#27, #28; Figure 20). 63 -?...-?-- --~--.£~ c======:::::~ Figure 19. Variation in head pores as seen in barbatus (above) andfehlmanni (below). 64 Analvses Phylogenetic analyses were carried out using PAUP version 3.0 (Swofford), with a heuristic search invoking MULPARS option with rooting was determined by outgroup. The number of taxa involved ruled out branch-and-bound and exhaustive searches. Because results may be sensitive to the order in which taxa are added to the tree, all searches were replicated 50 times using randomized order of input. Table 5 shows the data matrix analyzed. Character evolution within the clade was examined using MacClade, version 2.97.62 (Maddison and Maddison). Because 30% of the data were osteologic characters, misSing for P. stephensi, ditrichus, and magdalenae, these taxa were excluded from the initial analysis and placed on the cladograms later based on overall similarity of other characters. Similarity was assessed by running an unrooted phylogenetic analysis of just the Paraclinini. Only characters with no missing values were used in this analysis. The placement of these taxa is quite tentative due to the small number of characters may change when more data are added. RESULTS AND DISCUSSION The phylogenetic analysis found four most parsimonious cladograms of 154 steps each (Figure 21). The consistency index (CI) of these trees is 0.305. Because consecutive substitution of outgroups and combinations of outgroups yielded the same ingroup topOlOgy, in these and all follOwing figures the outgroups shown are Starksia, Xenomedea, and the hypotheticaloutgroup (the consensus of all the outgroup taxa). A strict consensus of the four most parsimonious trees is shown in Figure 22. Nodes are identified by letters that will be used in the remainder of the discussion. Three of the four 154-step trees (referred to as topology 1 in SUbsequent discussions) vary only in placement of P. altivelis and P. monophthalmus in relation to the Exerpes naeorhegmis group (Clade 3, Figure 21). The fourth tree (topOlOgy 2) is somewhat different in that it adds P. sini,fasdatus and mexicanus to the beebei-fehlmanni·tanygnathus clade (Clade 2, 65 Figure 20. States of anal fin membrane attachment; on caudal fin, extending the length of the ultimate ray (above); anterior to caudal fin, extending partially along ultimate ray (below left); and anterior to caudal, attached at base of ultimate ray (below right). 66 Table S. Data matrix analyzed in phylogenetic analyses. Character numbers correspond to those given in Table 4. Species States for characters 1-40 grandicomis 1 100 1 1 1 1 1 1 1 1 1 0 101 100 1 1 1 1 1 1 1 1 000 0 1 0 0 0 0 102 barbatus 1230111100111001211011000111100111100101 cingulatus 2101100110011002200000111100011010000112 fasciatus 2121100100111001200011000001010010110110 infrons 1220111101111110111101001111000111001111 marmoratus 1 2 3 0 1 1 1 100 1 1 101 000 1 100 1 001 1 1 100 0 1 1 101 100 nigripinnis 1120110110001012201101110001001000010002 naeorhegmis 2231110100011012200000000111001001111110 sini 2230100000001101200000010000010010111100 beebei 2220100000000102200001010000101010001010 mexicanus 1120100000011002201100010000010010100110 ditrichus I?? 1110??00001022 O??? ???O?OO?? 0010? ?0110 integripinnis 2010100110000012200000000001010000110100 walker; 2010100110000002200000010001010000110110 tanygnathus 2 2 3 0 1 1 0 1 000 1 0 1 022 0 0 0 0 1 0 1 000 101 101 1 1 1 101 2 altivelis 1230111000011112200000000001010001111000 magdalenae 1 ? ?0110??001100220 ? ? ? ? O?O?O 0??0111? ? 0 1 1 0 stephens; 1 ? ?0110??001010220 ? ? ? ? ??O?O 0??0010? ? 0 1 0 2 monophth. 1120110000000112201100000001010101100100 fehlmanni 2120100000000002200001110100111110001010 E. asper 11311 1 100 1 1 110 100 1 1 101 1 000 0 1 0 1 0 1 1 100 1 011 Starksia OOOOO? ?111011010100000?10100011110000100 Xenomedea OOOOO? ?111011010100000?10100001010000000 Labrisomus OOOOO? ?000000000000000?10000000000100001 M alacoctenus OOOOO? ?000000020000000?10000000000100101 .4.11oclinus OOOOO? ?000001010201100?0000001000010110? Hyp.outgr. OOOOO? ???? O??O?O?O??OO??O?OOO ??? ?O?O ??O? 67 Topology I Topology 1 grandicomis grandicomis barbatus barbatus inlrons Clade 3 inlrons asper asper marmoratus marmoratus naeorhegmis naeorhegmis altivelis monophthalmus monophthalmus ahivelis sini sini beebei beebei lehlmanni lehlmanni Clade 2 lanygnalhus lanygnalhus mexicanus mexicanus fasciatus fasciatus integripinnis integripinnis Clade 1 walkeri walkeri clngulatus cingulalus nigripinnis nigripinnis Starksia Starksia Xenomedea Xenomeclea Topology 1 Topology 2 grandicomis grandicomis barbatus barbatus infrons infrons asper asper marmoratus marmoratus naeorhegmis naeorhegmis altivelis ahivelis monophthalmus monophthalmus sini lasciatus beebei sini lehlmanni beebei tanygnathus {ehlmanni mexicanus lanygnalhus fasciatus mexicanus integripinnis integripinnis wakeri wakeri cingulalus nlgripinnis nlgrlplnnls clngulalus Slarksia Starksia Xenomeclea Xenomeclea Figure 21. The four 154-step most parsimonious trees. Clades 1, 2, and 3 are indicated above left, and with circles at the base of their nodes. 68 Figure 21). This entire group then forms a clade with the integripinnis-walkeri species pair (Clade 1, Figure 21), while nigripinnis and cingulatus exchange places at the base of the tree. As can be seen from Figure 22, for all I54-step trees the position of grandicomis and the nigripinnis-cingulatus pair is consistent (Node B), though the latter is unresolved. Clade 3 (5 taxa), clade 2 (3 taxa), and clade 1 (2 taxa) are always present and their positions seem to be stable. However, the relationships among these clades are uncertain, as are the affinities of fasciatus, sini, and mexicanus. This uncertainty is emphasized by the number of trees requiring just one more step. Eighty six trees are found when 155 steps are allowed. Consensus trees from this analysis are shown in Figure 23. Note that the strict consensus still shows grandicomis to be most primitive and maintains the groups barbatus-infrons-marmoratus and Exerpes as well as beebei and fehlmanni. However, all other relationships collapse into an unresolved polycotomy of 13 branches. The majority-rule consensus tree shows that the relationships found in the most parsimonious trees occur in 57% or more of the ISS-step trees. Adding the three taxa with missing data resulted in 4 16I-step parsimony trees, which of course are much less resolved than when no data were missing. The three taxa fit in at node F of a strict consensus tree (Figure 24). Node F is an unresolved polychotomy of 8 lineages, only two of which represent more than one species. This analysis indicates that these three taxa are not members of clades 1, 2, or 3, but they are more derived than clade 1. The unrooted analysis of only the subset of data that were complete for all ingroup taxa places ditrichus and stephensi as sister taxa with magdalenae as the next outgroup (Figure 25), with the sister taxon of these three as mexicanus. Rosenblatt and Parr (1969) discussed the Similarity of ditrichus to mexicanus, fasciatus, and cingulatus. They also thought stephensi and monophthalmus might be closely related, and that magdalenae shared some characteristics with the latter. Exploration of various placements of the three species suggested by these 69 Strict Qrandicomis Darbatus I infrons I asper DI marmoralus A naeorhegmis I- -""" altivelis monophthalmus fqsPatus e SIn! beebei fehlmanni tanygnathus B mexlCilnus. jnt~npinn!s wai Majority rule randiCOmiS arbalus rrnfrons -~-- asper marmoratus :!.£!~=~~======naeorhegmisaltivelis 100 r monophthalmus L-______~~-- g~~bei L____ ....!.!Ll!. ____-[=~== fehlmanni tanygnathus l_~====~;;======::: fascialu~mex~nus . L ------...... ;~:.....------C= wal Adams Qrandicomis Darbatus I infrons asper marmoratus J na.eomegmis altlVelis monophthalmus faSCIatus J I ~inlb • I I I re~i~~ni tanYQnathus I mexieanus ~~~:rinnis c!OQu!atlls nlQflPlflnls Starksia Xenomedea Figure 22 Strict, Majority rule, and Adams consensus trees of the 154-step trees in Figure 21. 70 Strict orandicomis Darbalus infrons .... asper .... - marmoratus cingulatus f~sqaJus. mgnplnms . n.aeorhegmls sim beebe I fehlrnannl mexicanus ~l?::rinnls laOYQflathus altiVellS monophthalmus StarkSia Xenomedea Majority rule ndiCOmiS 100 rbalus 100 100..r-- p;n rons 80 _ asper marrnoratus .... naeorhegmis ....E-J altivelis ...1QQ... monophthalmus f~~alus 57 slm 100 ___ beebe! . 86 56 fehlrnanm - lanygnathus 69 rnex~lJus I 98 Int~nplnn!s L wal Adams Qrandicomls Darbatus J lnfrons l ~ratus nae9rhegmls faSCIatus sinl tal1Y.gnathus bee6el • fehllJlanm mexlCanus ~l?:rflnnis altivelis monophthalmus cinauratus nigrlPi!"mis StarRsia Xenomedea Figure 23. Consensus trees resulting from the 86 trees found when 155 steps are allowed. 71 MajOrity~ru:.::.:::le ______100-;:::;;;;:::== grandicomiS r arbalus 1....:.=--r::== Inlrons r naeo egmls ~=:l~~~=~~~~~~~~ anrve~ IS us. 100 W;'l!n~UJ's 100 rna .Henae :1O:OJ~~~1~0~0~~~~~~i ste&i~~hrn ensl Dhlhalmus [ ;asaalus L------.....!~------_C=:: mfJ!,lnnis n loms ~ la ~=~~~==~~~~~~~~~~~~~~~~~~~ ~~IatusXenomedea AdamSr______~;===::: . gr,arWa~mls I--C== rnJrons naeo egmls [=j==~~~~~~~ ~ra!uye ISratus ~Imb . ...---lr:::::= re~i~h I 1------======IDIPr'ffrfsuStanlll'Jaffius a lenae L_~======~~;;;;~~- ~iL!flk,musas aus L------iC= m~1i.!Plnnls ~~~~~~.IalusI ms . ~ enomedea Figure 24. Consensus of four 161 step trees resulting from parsimony analysis including magdalenae, ditrichus, and stephensi, the taxa for which much data are missing. 72 speculations requires more steps in the tree than result from placing them together with mexicanus (Figure 26). I have not included these taxa in subsequent discussions and figures. I include them here for the sake of completeness, and draw no conclusions from this placement since there are many equally parsimonious topologies. Resolution of their relationships must await additional data. To explore the character states that support the two basic topologies for 154-step parsimony trees, I compared the Changes in CI for each character from one topology to the next. If the characters in which I have more confidence change less (have a higher CI) in one topology than the other, I would favor that topology as more likely. Six characters showed increased CI in topology 1, while four characters were less variable in topology 2 (Figure 21, Table 6). Four of the six favoring topOlOgy 1, (#2,9, 14, and 37) are mapped onto topology 1 in Figure 27. Of these six, #2, #14, and #37 support the monophyly of sini + clade 1, and clade 2. Character #9 strongly suggests that fasciatus and taxa higher on the tree share an ancestor, and characters #30 and #39 support a higher position on the tree for cingulatus than nigripinnis. Four characters show less homoplasy on topology 2 (Figure 28). Of these, character #26 is simply a retained ancestral state, #33 is a loss. Considering the type of character suppOrt for topologies 1 and 2, topOlOgy 1 seems better supported in that the characters which exhibit less homoplasy in topOlOgy 1 seem to actually support nodes rather than simply changing fewer times, as is the case for characters contributing more to topology 2. Paraclinus integripinnis and walkeri have been discussed a sister species previously. In their revision of the Pacific Paraclinus, Rosenblatt and Parr (1969) found very few differences between these two species. Except for the numbers of branchiostegal rays, some color differences, and shape of the opercular spine, the two are indistinguishable to the eye (although there are significant differences in sexual dimorphism between the two). Hubbs (1952) identified only two lineages within the Pacific Paraciinus that he revised; one of these was the 73 StriCi Clrandicomis I Daroatus I I inlrons marmoratus cia~ ulatus Ina.eo. '~s egmls . altwe IS l Majority rule aranclicomis 100 J 71 Darbatus 71 marmoratus 71 I 100 psoer I Il')rrQn~ • cinSamms Olalus 100 f ·~s . 100 na.eo. egmls 100 100 -.J altwe IS 100 l Adams Clranclicomis Daibatus infrons I marmoratus ci lJlalus laalf! ItuS . naeorhegmls altivelis J 1 Figure 25. Consensus trees resulting from an unreoted analysis of all Paraclinini. Note the change in position of grandicomis when there is no outgroup to polarize characters. i ~ ~ grandicomis 0 ::s (l) nigripinnis .....,0 :3 cingulatus ::sI\) '< integripinnis "0 0 Vl walkeri Vl CT ~ "0 j;;;' n (l) !3 ::s(l) r.;: ...,0' ~ 'mexicanus & 15- fehlmanni ::s~ ~ beebei ~"' l::l. tanygnathus ~ ~ infrons ,:-,a asper I\)::s 0. barbatus ~ marmoratus S. I:: !'> naeorhegmis altivelis monophthalmus sini -l ~ 75 Table 6. Consistency indices and number of steps for variable characters under Topologies 1 and 2. Character CI: Topology 1 ## steps CI: Topology 2 II steps #2 0.33 5 0.25 8 # 9 0.50 2 0.33 3 # 14 0.25 4 0.20 5 # 26 0.17 6 0.20 5 # 28 0.20 5 0.25 4 # 30 0.25 4 0.20 5 # 33 0.20 5 0.25 4 # 36 0.17 6 0.20 5 # 37 0.33 3 0.20 5 # 39 0.20 5 0.17 6 ·(z ~orod01 Ol gAHEigl) 1 ~orod01 1gpun I:J gsEgJJU! tp!qM sJglJE1EqJ X!S gql JO 1nod ·Lz g1~!d hypothetical ..-,.._ '"~""' ypothoOC. ...?"''""". . ,...._ ""''""' ~ b#// "'~::::-·~o . • tanygoath · ~w ID§w~ ! ~ QQ 3:;. 5- n •-it~~ 0 • ~- o o o a • ; • • -~ 3 ~~~~ ' ' ~ ~ -0 ;; .N '>iba hypothetical outgroup /{]hypothetical outgroup Xenomedea ,, ,, Starksia ~ ~· nigrip~nnis ~ #A"'""d""m" //// _,~··" cingulatus integripinnis walkeri JJ ///~wal~eri lasciatus mexicanus lehlmanni ///// f f ~lehlmanni beebei ""v tanygnathus sini ~ 10 i ~; altivelis liD i il ~-N~-g-g ii>3C.!-gi ~ ! i as per ~ Ci !: .a 0 - Ill 0 7<" 0 0 ~ - inlrons c: 2. ~ i - "'C ;) barbatus ::: "'7<" $ CD • ~ c: a ~ ~ marmoratus - AI naeorhegmis "'C"' & 5 CD monophthalmus N "' 9L 77 .cc, >. .c c !!! 0, .i> snwte414douow c u; ..!! >. !!! !!! ·a >. g> !!! n; c. 0 0 .c c c. t;j "' c IV .i> nl ..0 "' n; "0 c E £ (J ·o "5 IV Q) 0 0 c 0 ~ > Q) "0 .c E "0 .c Q) £ Q) n; 0 5 CT Q. "' ... "i "i c "' ... .c E "' Q. Q) Q) oCI>"O : ~E Ci u; 0 nl "' 0 c c -Q. &/") c:::) IV~ :::) 01~ 01 !9Q99q !UUeWj49J !UUeWj49J !U!S snue:>txaw snue:>txaw S!UU!d!J0aiUI SnletnOut:> 00 S!WO:>!pueJO \0 e!S>tJels e!S>tJeiS ~ ~ eapawouax eapawouax dnOJOjOO te=>!194i0dA4 dnOJOjOO te:l!l94iOdA4 Cl> Q. nl snwte414douow ~ E c :::) 0 S!W084JOaeu Q. ·£a; 0 0 nl )( !UUeWj49J IU!S snue:>!xaw sn1epsel pa>jteM S!UU !d!J0aiU! S!UU!d!J0a)U! S!UU!d!Jfl!U S!UU!d!Jfl!U sn)etnOut:> eapawouax• eapawouax dnOJOjn o te:l!l8410dA4 dnoJtlinO te:>!lB4iOdA4 Figure 28. The four characters with higher CI under topology 2. 78 integripinnis-walkeri pair while the other was the rest of the Pacific Paraclinus species known at the time. Rosenblatt and Parr, in discussing relationships of integripinnis and walkeri, did not go beyond pointing out similarities and differences of the pair to ditrichus, mericanus, and fasciatus. Because there seem to be equal numbers of similarities and differences, they were unable to form a strong opinion of clade l's closest relatives. The current analysis conservatively places the pair at unresolved node C (Figure 22), so many relationships are equally likely. Topology 1 would place clade 1 between cingulatus and fasciatus on the cladogram, with mexicanus removed by several more steps. The close relationship betweenfehlmanni and beebei (clade 2) has been previously discussed. Springer and Trist (1969) in their description of Paraclinus fehlmanni, state that the new species will key out to beebei on Hubbs' key to Parae/inus, and they identify beebei the closest relative of the new species. The main differences between the two seem to be in meristic counts, which are lower in beebei. Since beebei achieves a much smaller adult size than fehlmanni, these differences may be size related. The two species are also quite similar for all the head pore characters identified, sharing elaborations of some systems seen in no other species. Springer and Trist did not identify tanygnathus as being particularly close to beebei and fehlmanni while this analysis identifies it as the sister species to the pair. All three taxa share an elaborate supratemporal commissural pore P2 (also present in clade 1 and monophthalmus), the absence of pelvic threads (also characteristic of Clade 1,fasciatus, nigripinnis, and grandicomis), lack of scales on pectoral base and nape, and dorsal spine 3 of approximately equal size to the more posterior dorsal spines (this state is also seen in nigripinnis, alrivelis, and E. asper). By far the most interesting group identified by this analysis is clade 3, consisting of Exerpes, infrons, barbatus, marmoratus, naeorhegmis. Some of the characters unifying this clade and its subgroups are depicted in Figures 29 and 30. All five species show a general reduction ------79 in number and elaboration of head pore systems and a completely incised dorsal fin membrane (allivelis and monophthalmus also share this state). Exerpes, infrons, and barbatus are unique in the anterior position of the mouth; anal fin membrane attachment on the caudal peduncle rather than further anterior (except in Exerpes); state of the ventral post-cle~thrum (again excepting Exerpes); a simple point for a lateral process on the hyomandibular; and a strong conical opercular spine. Head shape in this clade is progressively more pointed (Figure 31), with the dorsal fin high anteriorly with an incision or at least lower 3rd, 4th, or 5th spines (barbatus is an exception among the 5 species, with a low even dorsal). The first three spines are located far anterior and heads tend to be more compressed than in other groups. Bohlke (1960), in his description of infrons, discussed the relative merits of placing it in Paraclinus or Exerpes, recognizing the similarity of infrons to Exerpes. Because Exerpes is so distinct, he conservatively put infrons in Paraclinus. Hubbs (1952), Springer (1955), Bohlke (1960), Springer and Trist (1969) and Rosenblatt and Parr (1969) were unanimous in their frustration at their inability to identify anything but possible species pairs and to discuss nested sets of characters identifying groups. All noted that one set of characters would identify one group, while another set of characters would unite entirely different taxa in entirely different arrangements. This indicates a high level of homoplasy in the characters they were using, and I had hoped that the addition of osteological characters would allow complete resolution. However, complete resolution is still not possible. Even when a character is fairly robust in defining a clade, it is likely to show up in the same state in a completely different portion of the tree. The amount of homoplasy is apparent in the very low CI value of 0.305. According to Sanderson and Donoghue (1989) this is less than the expected CI for this number of taxa. Even so, some conclusions from this study are fairly robust. First, grantiicomis, cingulatus, and nigripinnis are the most primitive members "£ gpB{;) aup1oddns SJglJBJBqJ gUJOS ·6z gl~!.~ hypothetical outgroup • hypothetical outgroup Xenomedea grandicomis nigripinnis •cingulatus integripinnis fasciatus mexicanus mexicanus sc ...:. J"' sinl § w ~ 10 a. Ci ¥ altivelis altivelis ~, rn1o aia CD "0 - ~ "' 0 !!!. "';r 0~ CD - as per ~ "8 asper 0. :g = 5" 3 ~ tO ~ - "2. !"'§ c.> in frons 0 ~ CD in frons ~ ~ -g ::: barbatus 0 barbatus ::> marmoratus •< a. marmoratus 0 ;r naeorhegmis ~ ~ ~ naeorhegmis hypothetical outgroup ~hypothet i cal outgroup Xenomedea tj//.1] Xenomedea Starl nigripinnis nigr,ipinnis cingulatus cingulatus integripinnis walkeri lasciatus mexicanus lehlmanni beebei rrn I 0 c "' s- sini I 0 c w ~~~ ~w~f ~~~::iygnathus WJ -· 0 1i ~ altivelis ~ i ~ vo~ ~altivelis D o ; "' :::. asper o Ill "' ::> -asper : . !2~ . ~ 0. ::> ::> :! ~ 3 /..., g ~ g· ~ infrons &l 0 ~ !!. o 3 barbatus a o r::r ~ o- !!!. Ill Ill ~ marmoratus :::. ~ := CD ::1 - 0 naeorhegmis 5. .g ~naeorhegmis monophthalmus monophthalmus 08 '£ gp-eJ:J JO sdno1a'qns a'up1oddns sJgl:JBJBq:J ·o£ gJmJt~ hypothetical outgroup hypothetical outgroup Xenomedea Xenomedea Starksia Starksia grandicomis grandicomis nigripinnis nigripinnis cingulatus cingulatus integripinnis integripinnis walkeri walkeri fasciatus fasciatus mexicanus mexicanus fehlmanni fehlmannl beebei beebei tanygnathus __ t~n.ygnathus ~ c: w 0 :::1 lJ 10 a~~ o ; en i IC:lJ~~Q 0 i i ~ ~~~::~~el i s ~=gill a_ (/) w :T :::1 ! CD cr "/"~·asper < 0 Ill l ~ a. ?i ~. i nfrons ~ !. a: CD - a_ lJ 0 q; naeorhegmis (/) "" "" ·-naeorhegmis monophthalmus monophthalmus hypothetical outgroup hypothetical outgroup Xenomedea Xenomedea Starksia Starksia nigripinnis cingulatus ~;ot~·~;oo ; , integripinnis walkeri walkeri ~-;aru, fasclatus mexicanus mexicanus ~fehlm~nni fehlmannl beebet beebe I tanygnathus sin I slnl rniiD!~i altivelis § N 10 0 (II ~CD ~ii~~~~~ altlvelis asper a. a>; ~ · ~ i l a. '< - · n !! ~- as per Q CD - · Ill CD infrons i ~ ~ 5" ~i~'< ~ ...... :::1- · (D barbatus c: c: ~; 0 g lJ 0 :::1 10 = i marmoratus - c Q Ill ~ (II ~ - ~ naeorhegmis marmora !us Q 0 lJ .. - monophthalmus naeorhegmis Ill g Q !!! monophthalmus g a-0 18 82 Exerpes asper Paraclinus infrons Parclinus barbatus Paraclinus marmoratus Paraclinus naeorhegmis Figure 31. Clade 3 illustrating elongated head and triangular dorsal fin shape. Compare this to nigripinnis in Figure 10. 83 of the clade. I would not be surprised if further addition of character evidence supported their monophyly. They are quite similar in shape, having rather broad, blunt heads, dorsal fins with a low, even margin, and extremely long jaws. At the other end of the tree, relationships are revealed that had not been previously discussed, naeorhegmis, marmoratus, barbatus, infrons and Exerpes forming a clade. I suspect that further evidence will show altivelis to belong within this clade as well. The position of monophthalmus is less certain, as there are many traits the rest of these taxa share that are quite different in monophthalmus. Of the unresolved group in the center of the tree, little can be said. I suspect that mexicanus and fasciatus are more closely related to clade 1, with sini perhaps as the outgroup to clade 2. The former have broader rounder heads and low even dorsal fins (resembling clade 1 and the more primitive Paraclinus) while the latter are shaped more similarly to clade 3, though not as extreme. Where the other unresolved taxa will eventually fit in is difficult to say. It may be that the three missing taxa will be key to resolving ponions of this tree. Finally, my analysiS indicates that Exerpes asper should be included within the genus Paraclinus. Placing it in a separate genus (which contains only the one species) makes Paraclinus paraphyletic. Because its closest relatives are members of Paraclinus and some Paraclinus are more closely related to Exerpes asper than they are to other Paraclinus, the separation is artificial and misleading. Nomenclature should reflect phylogenetic similarity rather than morphological differences; therefore I will refer to Exerpes asper as Paraclinus asper for the remainder of this manuscript. 84 CHAP1ER THREE EVOLUTION OF SEXUAL DIMORPHISM ABSTRACT' Sexual dimorphism in the tribe Paraclinini is examined here in a phylogenetic context, comparing character states and current ontogenetic growth patterns with hypothesized ancestral states based on the phylogenetic hypothesis from Chapter 2. Overall, dimorphism seems to be ancestral within the Paraclinini, particularly in characters from the head region. Within the clade, dimorphism very often decreases in the most derived species, occasionally reversing from dimorphic with males larger ancestrally to dimorphic with females larger. These changes seem most often to occur by neoteny in males coupled with acceleration in females. Decreases in amount of dimorphism also occur due to post-displacement of the size at which allometries for males and females diverge. INTRODUCTION Sexual dimorphism has been a matter of curiosity to biologists since Darwin first proposed that many secondary dimorphic traits evolve not by what he termed natural selection (which he generally seems to have focused on survival), but by sexual selection, where the advantage of a particular trait lies not in greater survival or resource gathering ability but in advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction" (Darwin 1871). Studies of mechanisms of sexual selection and theories for evolution under sexual selection have proliferated over the last 20 years, and these are by far the most commonly cited causes of observed sexual dimorphism (Slatkin 1984, Shine 1989). There are, however, other equally reasonable explanations for sexual dimorphism, including selection for ecological divergence (Selander 1966) and selection for different optimal 85 male and female fecundities. Another frequently ignored reason for current dimorphism is simply that of a dimorphic ancestor. These alternate hypotheses have been neglected in the rush to explain all sexual dimorphism on the basis of sexual selection hypotheses. In this chapter I investigate a monophyletic group of fishes in which sexual dimorphism is quite often present. Rather than propose selective reasons for the presence of dimorphism, I examine the distribution of dimorphism within a phylogenetic framework to determine whether particular cases of dimorphism can be explained by their presence in an ancestor or whether the change has been derived more recently. In addition, ontogenies of dimorphiC characters were used to evaluate whether evolutionary changes in the growth patterns leading to adult dimorphism were likely to have occurred in males, females, or juveniles or some combination of the three. MATERIALS AND METHODS Measurements Measurements were made on the maximum possible size range of males, females, and juveniles for all 21 species within the tribe Paraclinini. The measurement methods used are described in detail in Chapter 1. Distances measured are shown in Figure 2 and described in Appendix 1. Within each species I attempted to measure 45 specimens; 15 males, 15 females, and 15 juveniles. Sex determination follows methodology described in Chapter 1. Material examined The goal of 45 individuals per species was not always possible to meet, since some species are rarely collected and juveniles are always less common than adults in museum collections; even when present they are not always identified correctly. Specimens examined are identified in Table 3 of the previous chapter. Allometric models Particular growth models were fit to size series of specimens within each species as 86 described in Chapter 1. For some species there were not enough specimens to fit the models; for example in P. grandicomis I had only two juveniles, in alfivelis I had none. Other species were borderline sample size, and for these I fit the growth models then jackknifed the analysis to see how robust results were. These species are therefore problematic, in that even with results robust in the jackknife analysis adding individuals may change the results. Species for which sample sizes are marginal include fehlmann~ barbatus, and tanygnathus. Measuring dimorphism Qualitative determination of dimorphism, scored as presence or absence, seems simple enough at first glance. However, the traits we tend to recognize as dimorphic are usually extreme, and there are many more subtle characters that might be missed in a gross assessment. That a particular trait is not immediately obvious to human perception does not mean it is not important to the organism bearing it. While I have probably not solved the question of when to call a difference significant biologically, I have a clear protocol within the context of this research. Whenever pOSSible, I allowed the growth models to determine whether a trait is dimorphic. Any trait that fit model 2 or 3 significantly better than model 1 was considered to be dimorphic. The exception to this was those characters which fit model 3 best, but for which males and females diverged from the juvenile growth pattern with the same slopes. These cases were considered to be monomorphic. Although this allowed me to detect very subtle differences between males and females, it also made it difficult to compare dimorphism for those species laCking sufficient sample sizes to fit the ontogenetic models. These species were scored for the most obvious characters only, by eye. The result of this is that sexual dimorphism (in terms of the number of dimorphic characters) for grandicomis, naeorhegmis, and alfivelis is probably underestimated. Amount or extent of dimorphism was determined in twO ways, each with its own 87 weaknesses. First, the number of dimorphic characters per species was tallied. This ignores the amount of divergence between males and females as well as correlations among contiguous characters. Second, the amount of divergence was estimated using a 'scaled dimorphism index'. Differences between males and females are a function of both the differences in allometric slope and the size at which the slopes diverge. The dimorphism index is the average slope difference between males and females, multiplied by the number of dimorphic characters for a given region and the average "time" of divergence for that region. Slope differences and divergence points are derived directly from the fitting of the ontogeny models. Divergence "time" was estimated from the body size at which the male and female allometric slopes diverged. This formula gives a better index of actual difference between males and females, since a character may diverge with radically different slopes for a very short period of time and still be less dimorphic than one which has less slope difference but changes earlier in ontogeny. Multivariate analyses PrinCipal component (PCA) and discriminate analysis (DA) for each species with large enough sample sizes were carried out as described in Chapter 1. To explore overall shape differences among specie, a PCA of all species was also performed. In addition, character allometries (allometric coefficients) for males, females, and juveniles were analyzed by PCA to determine the major trends that were present. Relative allometries were calculated for each sex within each species by defining the average slope of all characters to be isometry. Because allometries are relative dimensionless measures, the PCA of allometries used the correlation matrix rather than the covariance matrix. Character evolution To examine evolutionary changes in particular characters or body regions of interest, selected dimorphic characters were mapped onto the hypothesized phylogeny of the Paraclinini. Relative allometric coefficients were averaged for four nodes along the tree. These nodes 88 Table 7. Pattern of sexual dimorphism within Paraclinini. M = male relatively larger, F = female relatively larger. Species are identified by letter abbreviations (see Table 9). g n c t w f m y z h s p a r b i x Head 1-7 M F M F F F F F F 1-8 M M M M M M M M M F M M F 1-6 M M M F M M M M M F F 7-6 M F M M M M M M 12-6 F M M M M M 7-8 M M M F M M 1-2 F M M M F M F 2-4 M M M M M M M M M M M 4-5 F F F F F F F F F F F 5-5' F F M F F M 4-4' M F M 3-3' M M M M M M M M M M M M M 2-2' M M M M M M M M Jaw 1-10 M M M M M M M M M M M M M M 9-11 M M M M M M M M M M M F F M Midbody 7-12 F F F F M M 12-13 F M F 13-14 F F F F 14-15 F F M M F F F 15-16 F F F M F F F 8-17 F F F F F F F F F F F F F F F F 7-17 F F F F F F F F F F F F F 8-16 F F F F F F F F F F F F 16-17 F F F F M F M M M M M 89 Table 7. continued g n c t w f m y z h s p a r b i x Post- body 16-30 F F F M F M M 30-31 M M M M 31-32 M M M M M M M M 32-17 M M 16-31 F M F M M F M F 17-30 M M M M M M M Med. Fins 7-18 F F F F F F F M 12-19 F F M F M F M 13-20 M F F F M M 14-22 F F F F F M 14-21 M M M M 15-23 M M M M M 32-33 M M F M M F M M 17-34 M M F F F M M M F Length 1-35 M F F F F M F F F 90 correspond to robust groupings within the clade, and these conclusions will not change when the phylogeny becomes better resolved. RESULTS AND DISCUSSION Summary tables Patterns of sexual dimorphism for all species are summarized in Table 7. By body region, it is apparent that head measures are more often relatively larger for males than for females (73 instances of relatively larger characters in males versus 34 occurrences of relatively larger head characters in females). The head measures for which females are larger tend to be those associated with length, such as the distance from the snout to the insertion of the first dorsal spine (character 1-7). Males have longer and deeper jaws (characters 1-10,9-11), broader and deeper heads (1-8, 3-3', 2-2'). For midbody measures, females are most often larger (67 of 153 possible occurrences, as opposed to 13 instances of relatively larger male Characters). Those midbody measures larger in males are body depth and some of the dorsal-spine interspace measures. Females again tend toward relatively larger size for length measures. In the posterior body, males are most often relatively larger. Mid and posterior body measures are likely not independent of one another, particularly if total length is monomorphic while body regions are variously dimorphic. Relative decrease of a body region in one sex would represent a tradeoff of the other region increasing in the opposite sex. This non-independence may also be occurring in the head region. Extreme expansion of the upper jaw probably requires larger post-mandibular bones and muscles to operate. Median fin dimorphism measures are about evenly split between males and females, with 28 occurrences of larger males, 25 occurrences of larger females. Total length may also be dimorphic, one sex being relatively longer than the other at a given measure of general size. 91 Table 8. Ontogenetic patterns characters. I = Model A; M = Model B, males divergent; F = Model B, females divergent; 3 = Model C. Species are identified by letter abbreviations (see Table 9). n c t w f m y z h s p r b i x Head 1-7 M F 1 M F 1 1 3 1 F M 1 F M F 1-8 3 3 M M M 1 M M F 3 M M 1 3 1 1-6 M F 1 1 1 1 1 M F 1 3 3 1 M F 7-6 1 F 1 1 M 1 1 F 1 1 1 F 1 1 M 2-6 F 1 I 1 1 1 1 F 1 1 1 F M 1 M 7-8 3 M 3 3 1 1 1 3 1 1 1 M 1 1 M 1-2 M M 1 1 1 1 1 F 1 1 1 1 1 3 1 2-4 M F 1 1 1 3 F F M 1 3 M 3 1 1 4-5 M M F F F 1 F M 1 M F M 3 1 1 5-5' M 3 1 1 1 3 1 1 3 3 3 1 1 3 1 4-4' 3 M 1 1 1 1 1 1 1 3 3 1 1 3 1 3-3' 3 M M M F 1 F M F 1 1 M 1 3 1 2-2' 1 1 1 1 1 1 1 M 1 1 F 3 3 1 3 Ja",· 1-10 M 3 M M M 1 3 M M M F M M 1 M 9-11 M M M M M 1 F 1 M ? M M F M F Midbody 7-12 1 1 F 3 M 1 1 F 1 1 M 1 1 1 1 12-13 1 1 1 1 M 1 1 F 1 1 1 1 3 1 1 13-14 1 1 1 3 F 1 1 1 1 1 1 1 1 1 M 14-15 F M F 1 F 1 1 1 1 F 1 1 1 1 1 15-16 M M M M M 1 1 F 1 M I 1 I 1 1 8-17 F M F F M F F F M F F F F F M 7-17 F M F F M F F F F F F 1 1 1 M 8-16 M M F F M F M F M M M 1 1 1 M 16-17 F M M M 1 1 M F 1 3 1 1 F 1 F 92 Table 8. continued , , t In' c 'mly I z I b I i x Ip 'r I I Post-body 'w 'f 'h 'S 16-30 M F 1 3 M 1 F M M 1 F 1 1 1 1 30-31 1 1 F 1 1 1 F 3 1 1 1 1 1 1 F 31-32 3 M F 3 3 1 M 1 F 1 M 1 F 1 M 32-17 1 M F 1 1 1 1 1 1 1 1 1 1 1 1 16-31 M 3 F F M 1 F 1 M M M 1 1 1 1 17-30 3 1 F F 3 1 F 3 F 3 M 1 1 1 F Median Fins 7-18 1 3 F F F 1 1 M F F 1 1 1 M M 12-19 1 3 M M 1 1 1 M 3 F 1 1 1 1 M 13-20 1 1 3 3 1 1 1 F 1 1 1 1 3 M M 14-22 1 1 1 1 1 1 1 M 1 1 F 3 1 1 F 15-23 1 1 1 1 1 1 3 1 1 3 1 3 1 1 3 32-33 3 3 1 1 1 1 1 M M 1 F M 1 3 1 17-34 F 1 1 1 F 1 1 F M 1 F M 1 1 1 Length M 1 1 1 M 1 1 M 1 M F F 1 1 M 1-35 93 Table 9. Abbreviations of species names used throughout Chapter 3. Paraclinus grandicomis g Paracinus cingulatus c Paraclinus integripinnis t Paraclinus nigripinnis n Paraclinus walkeri w Paraclinus fasciatus f Paraclinus mericanus m Paraclinus tanygnathus y Paraciinus beebei z Paraclinus fehlmanni h Paraclinus sini 5 Paraclinus alfivelis a Paraclinus monophthalmus p Paraciinus marmoratus r Paraclinlls barbatus b Paraclinlls infrons Paraciinlls naeorhegmis e Ererpes asper x 94 Females are relatively longer in seven species, while males are relatively longer in two. Table 8 represents the ontogenetic pattern with which each of these characters grows. Comparing Tables 7 and 8 yields no particular pattern of correlation among growth trajectory and exaggeration of a trait in one sex or the other. Characters that are relatively larger in females may result from males diverging with lower growth rates, females accelerating growth rates, or from both sexes diverging from juvenile growth, as discussed in Chapter 1. There is certainly no overall pattern of male divergence from a juvenile to female growth curve, as was previously postulated for sexual dimorphism in general. This is in direct contrast to the chaenopsid blenny Coralliozetus angelica, in which for the most part males diverge from juveniles and females resemble juveniles (Hastings, 1991). Because the morphometric data were not analyzed in the same way, it is possible that the differences are due to differences in analyses. However, something entirely different may be occurring in chaenopsid blennies. Many species have dimorphic traits that are more exaggerated than those seen in Paraclinus. A comparative study certainly seems worthwhile. Selected characters: dimomhism. ontogenv. and evolution Because general trends are difficult to pick out and the growth patterns vary so much both within and among species, I will discuss a subset of the more commonly dimorphic characters individually by region. These characters are mapped onto topology 1 (see Chapter 2, Figure 22). My reasons for choosing this topology over topOlOgy 2 are discussed in Chapter 2. Head region Within the head region, there are 15 distance measures, all of which are dimorphic in some species and most of which are dimorphic in at least half the species. From these I have selected the five most commonly dimorphic characters to discuss individually in detail in terms of 1) the particular pattern of sexual dimorphism, 2) the ontogenetic paths leading to dimorphism in adults, and 3) the probable evolutionary history of the character within the clade. 95 divergence - 2M 3 2M 2M 2M 1 2M 2M 3 2M - 2M 1 2M 2M - 2F dimorphism M M M M M M 0 M M M M M M 0 M M M M ::I'" en en en e d en .i:'" ::I'" ::I C; .., .c -' .~ ·s .i: ::I ::I .i: d .c -.:I '" en -' .., '" d 0 .s.= d .... tJ .... :I .~ .., ::I ... .c ·en .s.= d .;:: ... -' =d =d .... 0 .c e'" d tJ CIJ Q; c d '" 0 0 .:.: :a .;:: -; tUl .;:; ~ ... 0 E ...... c tUl .:.:'" U e ~ >. ~ G) ~ ... 0 "'" d tUl C .... C; 0> CIJ CIJ C .:: ... d =0 = S ... "" :a CIJ ·a .... en d ""d ~ oS ~ ~ ~ ·en C; CIS"'" .&J 8 ><'" en "" -= ·u .s e .s = e X allometry 1 ~ 0.92 el1.14 , J 0.92 ,----- 2 ~ 0.94 el1.17 , J 0.94 '------3~ n~ eI 1.29 " , J 0.95 ------4 ~ 0.94 eI 1.36 MAXILLA LENGTH (1 - 10) J 0.99 Figure 32 Pattern of ontogeny, dimorphism, and mean allometric coefficients for character 1-10. 96 Paraclinus cingulatus Paraclinus barbatus Figure 33. Range of upper jaw lengths illustrated in barbatus and cmgulatus. 97 The two measures of maxilla length and width (characters 1-10,9-11) are among the most interesting as well as being the most extremely dimorphic. Male paraclinins are almost uniformly relatively larger than females for maxilla length (Figure 32). The two species mexicanus and infrons are monomorphic. It seems clear that dimorphiC jaws are the ancestral condition for the clade, but it is also evident that this dimorphism has been much modified within the group. Species at the base of the phylogeny, grantiicomis, nigripinnis, and cingulatus are among the most dimorphic in terms of difference between males and females of comparable size. These species have jaw lengths extremely exaggerated in larger males (Figure 33, above) while clade 3, represented by barbatus in Figure 33, shows the least difference between males and females. This trend of generally decreaSing jaw dimorphism within paraclinins is illustrated by the average allometries at four nodes in the phylogeny (Figure 32). Values represent the average male, female, and juvenile allometric coefficients for all species above the depicted node. Male relative allometries show a steady decrease, from high values of 1.36 at the base of the tree to the lower value of 1.14 for the most derived group. Females, in contrast, retain practically identical allometry for all major groups. Juveniles, similar to males, have decreaSing allometries but the decrease is much smaller (allometries change from an average of 0.99 to 0.92 for juveniles). Growth rates for juveniles are more similar to those of females for most species. Thus, the decrease of upper jaw dimorphism within the clade seems to be caused by neotenous changes in males rather than acceleration in females. The general growth pattern for this trait seems to be model 2, with males diverging from a juvenile to female trajectory. However in two species, tanygnathus and cingulatus, males and females both shift allometry relative to juveniles. In these species juveniles show isometric growth or slightly positively allometric growth. Males shift to a higher positive allometry, females to a negative allometry. Both these species have extreme dimorphism for this character ------98 and both are smaller than most of the other species as adults. Perhaps in order to achieve such a large jaw as an adult the growth must begin at an earlier stage than in species which grow for longer periods of time. It also is possible that the exaggerated jaw is partially a result of evolutionary change in juvenile growth rates while adult males and females retain the ancestral rate (Figure 34). If this were the case, the result would be a more extreme trait in adults but with the change occurring in juveniles; juveniles would be accelerated relative to ancestral juveniles (sensu Alberch et al). The extreme trait might have less to do with selection for adult function than with selection for juvenile function. Hypotheses explaining a condition in terms of selection on adults ignores selective pressures acting on juveniles. It seems that these alternate hypotheses should also be explored. Differences between sexes as adults are sensitive not only to growth rates of males, females, and juveniles, but also to the point in the individual's growth at which allometries change. If male and female allometries are similar between two species but the size at which they diverge is different, the adults of the species with earlier divergence will be more extreme in dimorphism (Figure 35). Evolutionarily, this is post-displacement (Alberch et al) if the divergence point occurs late (at a larger size) relative to the ancestor, pre-displacement if it occurs earlier. At least some of the decrease in amount of jaw dimorphism is due to such shifts in timing. On the average, for jaw length the allometric divergence occurs at 47% of largest adult size. Both beebei and marmoratus diverge earlier than average, at 32% and 36% respectively. Conversely, asper, though dimorphiC for this trait, does not show divergence between males and females until 78% of largest adult size. Differences in amount of dimorphism due to post displacement in asper are evident when comparing this species with one which diverges earlier (Figure 36). In addition to shifts from juvenile to adult growth patterns there are probably shifts from larval growth patterns to juvenile growth patterns. These two are likely to be quite 99 Ancestor .c Q -..C ..L. mal. u female -a L. a .c u Q o ..J luv.nll. Descendant .c male Q -C .. female ..I. u -a I.- a .c o Q o ...I juvenile General Size Figure 34. Exaggerated trait in adults resulting from acceleration in juveniles, but requiring no change in adult allometries. 100 Ancestor Pre-displacement Descendant ..t:I ~ taD ...=II) ...... Post-displacement Descendant ...... -;..c:;.. ~--- Divergence size General size Figure35. Exaggeration and reduction in amount of sexual dimorphism resulting from pre- and post displacement of relative size at allometric divergence from juvenile growth. Paraclinus marmoratus Paraclinus asper Figure 36. Adults of mam20rarus and asper showing extreme dimorphism in the former, reduced dimorphism in the latter. 102 different; the shift from juvenile to adult patterns is likely much less extreme than larval to juvenile transformation. By the time the larvae settle form the plankton, they show basic adult characteristic shapes. A newly settled asper is unmistakable, and would not be confused with a newly settled naeorhegmis or cingulatus (Figure 37). Jaw width (Character 9-11, Figure 38) shows a similar pattern to jaw length in that it seems to have been dimorphic ancestrally with males relatively larger, but has undergone subsequent decrease in amount of dimorphism. It is quite interesting in that it has actually reversed dimorphism within clade 3 so for two species, infrons and barbatus, females are the relatively larger sex. Figure 39 depiCts this character plotted against general size for six species, four of which represent clade 3 and two of which represent a more primitive condition. Both of the primitive species, cingulatus and nigripinnis, show females and juveniles growing at the same rate with males diverging in a fairly extreme way. Female allometric coefficients for all species are fairly similar, between 1.05 and 1.26. Allometries for males, on the other hand, vary much more widely, from a low of 0.83 in barbatus to a high of 2.38 in nigripinnis. In all cases, male allometries are lower for the more derived species. The two species which show reversed dimorphism have extremely low male allometries relative to their outgroup, marmoratus. Paraclinus barbatus, in a rather interesting twist to the usual way of thinking of neoteny, juveniles as well as males are neotenous relative to the inferred ancestral state. Plotting both jaw characters for all species on the same axes reveals clear species differences in absolute growth rates (Figure 40). Primitive species share uniformly high growth rates for both these characters while the more derived species of clade 3 tend to have lower absolute growth rates. The remainder of the species lie between these two extremes. The fairly extreme jaw dimorphism is ancestral in the clade and the trend within paraclinins is toward decreased jaw dimorphism. This evidently is a result of neotenous changes in ~ales, some acceleration in females and post-displacement of the point of allometric ------103 Paraclinus asper 10.12 mm SL Paraclinus naeorhegmis 11.86 mm SL Paraclinus cingu/arus 11.51 mm SL Figure 37. Juveniles of three paraclinin species. 104 divergence . 2M 2N. 2M 2M 2M 1 2M 1 2F ? . 2F 2M 2F 2~ . 2M dimorphism M M M M M M 0 M 0 M M M M F F M M M :;:I...... en e ... ·2 :;:I :;:I a; ...... c: -' ·s ·2'" :;:I =s ·2 ..c: "C'" .... en ctI ... ctI -' = ctI l 8 c d ·a =s .2l =s ..0 ..c: .;; .;: ';: oW'" = = c oW ..c: r:>. e'" :c ·a :; ------4 ~ 1.13 cI 1.57 MAXILLA WIDTH AT DISTAL END (9 • 11) J 1.15 Figure 38. Pattern of dimorphism, divergence, and mean allometry in character 9.11. 105 0.5 0.0 Paraclinus infrons Exerpes asper .z: -0.5 Q. 0.0 R.latly. allom.try R.latl•• ellom.trl•• -e 1:1 "Q f + I = 1.28 m+I=1.10 m = 0.98 ,g -O.S -1.0 f • 0.97 X g -1.0 -1.5 E ~ g) 0 ...I -1.5 -2.0 -2.0 -2.5 -3 -2 -1 0 2 -2 -1 0 O.S 1.S 1:1 .z: Pa.ra.clinus ba.rba.tus ... d" Pa.ra.clinus m.a.1'1noratus Q. •• 1:1 1.0 -., 0.0 Reletly. allam.trl•• "Q m + = 0.83 t 0.5 ,g f • 1.14 X D -0.5 0.0 E at -0.5 0 ...I -1.0 -1.0 -1.5 - -1.5 -2 -1 a -2 -1 0 2 0.5 _------. 1.0 ..,...------. Paraclin1LS nigripinnis .z: Pa.ra.clinus cingula.tus . 0.5 . C. 0.0 R.latly. allometrl•• .. R.latl". allom.trl•• f + I ,. 1.0& og• f+I=1.19 I.'" 0.0 m :a ..... 2.38 ,g -0.5 m = 2.27 -0.5 xg E -1.0 -1.0 at o ...I -1.5 -1.5 -2.0 ""-_r--r---r--r---r---l -2.0 ~-r=---..,...--.....,---_--I -3 -2 -1 o 2 -2 -1 o Gen.ral slz. General slz. Figure 39. Scatterplols of logtransformed character 9-11 against general size. Neoteny in males, acceleration in females. and post-displacement have resulted in less dimorphism or reversal in clade 3. 106 Jaw Length .- o Z8"7' ••• P. "",",~.h&a p . • "'".Ju Slope. of the other .peeie. lie hetween 2 and 3 Jaw Depth --...... General Size Figure 40. Some of the slope and intercept differences among species. 107 divergence. Conversely, the ontogenetic changes that produce adult dimorphism are primarily acceleration in male growth relative to female and juvenile growth rates. In explaining jaw dimorphism in these fish, the appropriate focus is not understanding why jaws are generally larger in males, but rather what forces or neutral processes lead to concurrent neotenous changes in males and acceleration in females. There are five measures of head length, three form the lateral plane and 2 from the dorsal plane. Summaries for these characters are given in Figures 41 and 42. Distance from the snout to the first dorsal-spine insertion is dimorphic in about half of the species, and is most often larger in females. Given the spotty distribution of character states on the c1adogram, it is difficult to say which condition might be ancestral. The most primitive species, grandicomis, is monomorphic while the next two, cingulatus and nigripinnis are dimorphic. Paraclinus nigripinnis, however, has relatively larger males while in cingulatus the reverse is true. The lack of any very clear trend for this character is reflected in the average allometries, which are fairly similar at all four nodes in spite of the fact that the character has rather different manifestations at the termination points. Character 1-6, snout to opercular spine, shows a similar pattern of mixed dimorphism. This character is primitively and most often dimorphic, with males larger, while clade 3 shows reversal to dimorphism with females larger. Male allometries are decreasing from primitive to derived while female and juvenile allometries remain approximately the same throughout the clade. Character 1-8, distance from snout to pelvic insertion, is quite different. It is almost uniformly relatively larger in males. One exception to this is infrons, which has this character reversed with females larger. The closest relatives of this species are monomorphic. The general evolutionary trend in this character is for females to retain approximately the same allometries while primitively, males, begin with relatively high growth rates and show a decrease in these diva'g:c:nce 108 dirnorrtUsm .!O .!O ] 1! 8 II I! !1. 8 g " 'ii, " ~ .!! II :;; ~ " :! .z 'S ~ ;; ii ] :: :3 ~ ~ ~ ~ it j I j .; -; :I B i ~ ~ Ci 'iI ~ ~ S ~ oX ~ i ii ~ Xallometrv --- \ 0 0.86 d' 0.79 J 0.9\ ',----- 2 i 0.86 r:I 0.82 J 0.92 divergence ',------3i U~ dimo!phism r:I 0.84 , J 0.88 II ',------4 i 0.82 .!! .!! II 1! r:I 0.85 5 0g ] :9 'ii, II ~ HEAD LENGTH (1-6) J 0.89 ii 8 ~ 1: .3 " B c.. ~ " =S :! ~ g :: :g 'Eo .~ ] ~ -a it ,g ~ t ~ ~ i ~ .9 .3 B ~ ~ 5. :i u ~ . ~ s ~ .li ~ ." ~ :I a 1 Xallometrv - ---I~ r:I 0.71 , J 0.73 ,----- 2 ~ 0.82 rI' 0.73 J 0.76 ',------35! 0.82 rI' 0.75 , J 0.76 ',------4 5! 0.83 rI' 0.77 HEAD LENGTII (1- 2) J 0.77 ~~_r,_~~~_r,_~~_r~~~ divergence dirnorpl1;'" X.llom",. --- 1 5! 0.92 rI' 0.90 J 0.96 ',----- 2 5! 0.93 rI' 0.93 , J 0.88 '------J~ mss rI' 0.98 J 0.92 ,------4 5! 0.88 rl'1.02 HEAD LENGTH (1 - 8) J 0.91 Figure 41_ Three lateral head characters showing divergence, dimorphism, and mean allometries. --_._------divergence 109 dimorphism ., ., :> ., ~ ., ., .~ ~ ~ ~ ~ 8 ;:; ~ ;:; .. f .c 'a. .. .. ~ .!3 0 ~ :c 8 ~ "- ~ ::a 's. .E B eo ~ ~ of 0 ~ " ~ 'Ea e j >. 1i ,g ~ c ;I " '5. c ~ ~ :2 ~ x -=en ~ divergence dimorphism .. :> ., .!! ., ., .!! .. c :> .3 ~ .. E c :; -;; :: :: 1: .. 8 c c .!! .. l! ~ :;; ~ :~ " .. ... § -'" '" °5 ~ ~ ~ § 1- :~ ~ :t' ... .~ .~ e :8 >. ,g" :5 .. " :2 -;; K. ~ § .;:; .. .:l ~ ] .!l" .;;; A >< en S 'c " :9 "' e , ~ :J .:: -= e " S X allometry - --- 1 !j? 0.91 r:I 0.75 J 1.08 ',----- 2!j? 0.95 r:I 0.69 , J 0.99 '------3!j? 0.91 r:I 0.67 , J 0.84 '------4!j? 0.93 r:I 0.66 DORSAL: PREOPERCULAR MARGIN - OPERCULAR SPINE (4 - 5) J 0.80 Figure 42. Divergence, dimorphism, and mean allometry in dorsal view head characters. 110 rates for the more derived species. This trend seems to parallel that of jaw dimorphism, and the two are probably dependent. It may be that to support the exaggerated jaw seen in the more primitive groups, it is necessary to retain the rounder head shape and locate the jaw more ventrally. As the exaggerated jaw disappears, the bead is able to become more elongate with a terminal snout (Figure 33). Possibly the causal relationship is the reverse, with the head shape forcing a particular reduction in jaw size. The dorsal measures of head length discussed here are most often dimorphic (Figure 42). Females are the relatively larger sex for preopercular margin to the opercular spine (character 4-5) while the adjacent measure, orbit to preopercle (2-4) is always larger in. males when dimorphic. Again, dimorphism decreases in more derived species, although the trend is not as clear as with other characters. since 1/3 of the species are monomorphic for these traits. Male allometries for character 4-5 are, on average, much lower than those of females and juveniles. The more derived species tend toward acceleration in both males and juveniles, while female allometries are roughly the same. Character 2-4 shows marked neoteny in juveniles, slight neoteny in males and females. Females and males retain about the same average difference (0.05) in allometric coefficients above node 3. Between nodes 3 and 4 there is a large decrease in this difference. Species below node 3 are more dimorphic for this trait than those above node 3. Almost all of the head characters are negatively allometric (with allometric coefficients of 0.9 or less), whether dimorphiC or not. This reflects the differences in proportion seen between adults and juveniles. Since juveniles begin with relatively large heads, growth must be slower in the head region to account for the relatively smaller heads of adults. Figure 43 summarizes the number of head characters dimorphic for each species (out of a possible 15). Males are much more often larger for head measures than are females; though there are some exceptions (in frons and sini). The most derived group (asper, barbatus, and infrons) within the clade also shows (as a group) the least dimorphism. Total number of characters is not necessarily 111 Head and Jaw , 3 characters 0 ~ 10 . c.. ~ 0 co 8 E ~ /I) -~ .... 0 6 0 0 ~ I'" -~ 0 4 /I) ~ .Q 0 E 2 :l I Z 1 1 0 ~ 1 ,:1 1 I~ 11 en ::J en E en en n1 en en ::J ::J ·E ia OJ en ~ ·E en en ·c ::J ~ C> "0 ::J c: en ·c en Cii Q) .1: OJ 0 ·c c: c: Cii ::J .... n1 u ::J .~ rJ) 0 ~ c. c: Cii :§. .~ ca ·05 c: .... E ·en .0. Cii ~ C> Q) c: Cii E 0 0 ~ '6 "S E .0 Q) 0 0 c: c: .~ ~ ~ ·0 ·x >. Q) c: C> Q) Q) c: a. .... -E ro 0 Q) ro C> C ia en CD ~ CD ·c ~ en m n1 ~ .0 E c: E x Ci5 C> ·c ·0 ~ .!2 E .s? .c !9 ·en ia ca £ == Figure 43. Summary of total counts for dimorphic head characters. Left column = males relatively larger, right column = females relatively larger. 112 the best indication of amount of dimorphism, as discussed previously. Scaled dimorphism index, which takes into account the number of characters, and the actual amount of difference between males and females, is shown in Figure 44. Dimorphism is very clearly quite pronounced in the primitive species, and is lowest within clade 3, particularly in the three most derived members. These figures do not reflect qualitative changes, and it is critical to bear in mind that some of these clade 3 species have reversed dimorphism relative to the other species. Within the head region then, dimorphism has decreased markedly from the ancestral state, much of the decrease has occurred through neoteny in males, with females showing much more conservative allometries. This is quite interesting in relation to some more traditional models for evolution of sexual dimorphism. For example, sexual selection for exaggeration of a trait may be opposed by some survival cost to having an enlarged trait; many scenarios envision sexually dimorphiC traits balanced this way between natural and sexual selection. If this were the case, and sexual selection were relaxed, then the trait might be expected to reverse if it were still under natural selection. It may be that this is what has occurred in these fIShes with extreme jaw dimorphism. Midbodv dimorphism Midbody measures are, in general, dimorphic with females relatively larger (Figure 45). There seems little doubt that this is the primitive pattern, and again it is modified within the clade. Character 7-17, for example, shows very similar allometries at all nodes for males and juveniles. Females, however, show a steady neotenous decrease in allometry for this Character, the result of which is monomorphic species within clade 3. Paraclinus asper seems to re-evolve dimorphism in this trait by acceleration of females and juveniles, though ontogenetically males of this species diverge via neoteny. Character 8-16 is very similar to this. In contrast, character 8-17 does not seem to have been modified much. Females all have high pOSitive allometries while juveniles and males grow isometrically. Exceptions are asper and cingulatus, whose juveniles match females for high growth rate and whose males have unusually low rates. That this 1.2 13 Head 1.0 ~fidbody 0.8 0.6 0.4 0.2 0.0 0.2 0.0 1.8 ~ Total Dimorphism 1.6 1.4 1.2 1.0 0.8 ~ 0.6 ~ 0.4 h 0.2 0.0 n c t w f m y z h s p r b i x Figure 44. Summary of scaled dimorphism index for all species within four body regions and totaled. 114 I~~~el 5~~ ~~§ ~ci ~ ~p~ §§~ :~5 :~~ §§: 0<"0 _ I; ~f~: 0'''0 _ 00"0_ 00"0_ I~ ~.~: 00"0- 00"0 - =0 cnW,lqlqdoUDUI .., .., I .... I "- cnlUI'Qlqdouow I ~ I I I ::l: I I I I I I "- '!W'~\{J~CU I I I I =0 I I I I I I e C"ltJOWJtW I I I I ... ::l: I .... I SQleqJrq I I I 0 I I I =0 I I I =0 CUOJJO, I "- I I , .... ::l: I I "- J;)dSf I I I , ::l: I "- 'n~Am' , .., ::l: , I E' , I , "- U , E , .... "- l !' , ~ ...."- "- cnQltuJ.cUtl u. t ~ "''1'>11 ,au.wlq~J >- Q~ "- !uueUII'I:;!J Q ~ cnur'!%~w >- "- 0 Q .... "" cnUC!J::lW eItl enl'lXtJ 0 ~ ... '"lC!:'ISrJ ::<: ,J;'I'" Q'" u. i ~ IJ:'11" ,!UUld!J2~la1 "- N "- ,!uu!d!J2~lUf enlt1n'u!;) ::l ... ,nlt ln'U!' ~ ... '!Du!dpJ,a ~ ... ,!uu!d!J'IU ... '!WD.)!puuJ "UIOJ!PUtJ' '" r'C~JtlS 1:!'111:15 ~ E ~. ! .~~wouax e;lf!;uuOU:lX ~ ~. 'S ! .;; i :;"'.., "'.., '" ....C!~~ "'''' • c_~ C! ~~C! ,,",," - -"" _= __ -0- _"'0 -""~~C! - ... JI§~3 g:::~~>1 "':::i"': -0- ~~~ ,)( 0<"0 - 00"0 _ 0+"0 _ - - -- .,."0 _ .., 00"0 - I~ o.~- 0'''0_ 0'''0 - CnWIII\(lqdoucun .., I I CnWII:\{l'ldOIlOIU , , !:!i ... I , '1w'2)\{J~tU , , , I ... 'IUI')qJ~CU , , "'l1:JowJtW ,I ,I CnltJDwJtW , C"ltqJeq , , !:!i "- , , , , C"ltqn:q , cUOllUI I l!; , , , , ~ "- CU01JO! , , J~S' , , ... , , , , ~ J~~' , '!1:1Am' , , I '!1:1Am' IUrs , , I !: , , "- IU,I$ , ~ N "- e "'tnru2Iull ~ "- CMn'U,.cUI1 pcpaq e § >- !:!i "- pCp)Q luultnl'PJ Q z 0 ~ ... !UU1!UIIIPJ I cnuCJ!x:;lw !S Q cnutJ!X:;lW >- '" ~ ... Q '"l1!!:J;tJ 0 Si ~ u. C"ltPs:tl !J:;l'llc. '"Q ... !J:;l'll'· ~ c!uu!d~J'.:;lIU! "-N c!uu!d!l'.:;llUJ C",t:ln2up ... 'nltl"'u!~ ,!uu!dlJ'!u ~ !:!- ~ u. C!uuld'P'lu 0 '!WO:JIPUIJJ c:: S!Wo.1IPUIJ1 t!,:,nlS ~ E '1$:'V~IS !;. '.:;l~IOU:tX ~ ~ W:;lP:;lW('iU.:;lX ~ ~. ~ 'S f .;; ] Figure 45. Dimorphism, divergence, and mean allometries for four midbody characters. 115 character is so conservative suggests selection acting in the same direction with some strength. An increase in this distance, along with all midbody measures, would increase abdominal cavity size, perhaps allowing greater fecundity. This is more critical for females than males, since eggs are so much larger than sperm. Character 16-17 is a midbody measure that.indicates body depth at the origin of the anal fin. This distance, rather than being consistently larger in one sex, is quite mixed; split fairly evenly between being relatively larger in females, males, or monomorphic. In this case though, it seems that changes in males are primarily accounting for the differences within the clade. Female allometries are all fairly close to isometry or slightly positively allometric. Males show a rather marked increase in allometry from primitive to derived, resulting in some species with relatively larger males. Juveniles show a similar increase. This may reflect changes occurring in conjunction with deepening and shortening of the entire body. Primitive paraclinins are longer and more torpedo shaped, while the more derived species are shorter and deeper bodied. Distribution of midbody dimorphism within the clade for number of (:haracters is given in Figure 46 and for scaled dimorphism in Figure 44. Total amount of dimorphism decreases steadily from node 4 to node I, showing a similarity to head characters with more dimorphism primitively. Clade 3, above node I, tends to be monomorphic for many of these measures (Table 7). This reversal has primarily occurred through neoteny in females, occasionally acceleration in males and juveniles. Ontogenetically, most of these measures become dimorphiC through female acceleration. Again, as with head characters, there is no necessary correlation between changes from an ancestral state and changes from the juvenile state. Posterior body measures Two of the six posterior body measures are detailed in Figure 47. These measures are very mixed for dimorphism, with a trend toward monomorphic species to be clustered at the top of the cladogram. However, there are several monomorphic species that are relatively primitive. 116 M'dbody 0 9 charact.r. -c. ~ 8 ~ 0 E" 0 -a.-~ -u 00- 4 .0~~ .a~ E U 2 :J Z 0 rJ) ::s rJ) E (/) rJ) ctf rJ) (/) cu (/) ::s ::s "e Q) (/) II) "i:: .r:: .r:: II) 0> "0 "e II) ::s "i:: co Q) ::s c: ~ Q) 0 "i:: c: c: iii ::s 1: ctf u c: "5. ".:::: ::s ctf c: "~ II) 0 .r:: a. co ctf "Qi ~ n; 0 E "en "5. ".:::: Q) co u C> Q) Q) c: E 0 0 oX: =0 "S 0> E .0 .0 ~ c: c: ".:::: 0> oX: "0 "x Q) >- CD c: Q) II) Q) c: "i:: a. e co 0 Q) ca 0> c: co ::c: Q) ~ II) ca co fE .0 "en CIS CIS ~ .0 E c: E X Ci5 0> "i:: "0 £ == ~ E ~ .s Figure 46" Summary of number of dirmophic characters of the midbody region for Paraclinus" Left column = male relatively larger, right column = female relatively larger" 117 divergl'llCc dimorpllilm .. ~ " .~ ~ .. .~ ~ :! a .~.. '" .. a :S " a .c: "Z . 8 c " "c .!I .. :I' :;; ~ .. :l ~ Co ] :0 a. '5 ~ fl " f. of 0 c~ c ]. ... ;; 8 ] .... ,g" l: ~ c: E 'S. ~ ... ] ::;; i3 ~ K ~ ~ Eo c .~ ~ ~ .:l" -;; ;; :I '" :s • a J .s .3 S " S Xallomelry I 51 1.05 rI' 1.05 J 1.02 ',----- 251 1.02 rI' 1.03 , J 1.03 ,------3 51 1.01 rI' 1.00 J 1.02 ,------4 S! 1.03 rI' 1.01 POSTERIOR BODY LENGTH (16.30) J 1.04 divergence dimorphilm .. " .!I .. .. .!I .~ ~ .~ c .:: .c ~ .. . a c a " .. i! 'a, "c c: ~ .!I 0 & '" 8 " ~ '1: c .. :l of :0 " ]. '5 ~ .g S ] ...... !! ic ~ c :~ :I' .~ ::;; c K ,g" .e :; ~ l! ~ .;;a ~ ';:; ~ ~ .:l l: 8 S >< en .. ~ :s • a J ~ :: .s " XaliomellV - --- I S! 1.02 rI' ].05 J 1.04 ',----- 251 1.00 rI' 1.03 , J 1.02 ,------3 S! 0.97 rI' 1.02 , J 1.06 " ,------4 51 0.98 rI' 1.03 POSTERIOR BODY LENGTH (32.31) J 1.08 Figure 47. Dimorphism, divergence pattern, and mean allometry for two posterior body length characters. 118 Allometries do not show a clearly defined pattern, varying around isometry for the most part. Growth patterns are also quite mixed. Whatever the ancestral condition for these characters, there has been so much SUbsequent modification within the clade that any pattern is obscured. The posterior region is more often larger in males when dimorphic. This may reflect the presence of dimorphism in the anterior complementary measures. For example, if males and females are monomorphiC for total length, increasing size in character 8-17 must be offset by a relative decrease (within the increasing sex) in character 17-31. In general then, posterior body dimorphism (Figure 48, 44) show no clear pattern except to be larger in males somewhat more often. There seems to be no particular trend for dimorphism to decrease evolutionarily. Dorsal fin characters Median fin characters showed some quite interesting patterns both in terms of dimorphism and ontogeny (Figure 49). When dorsal spine lengths are dimorphic, they are most often longer in females. This is quite different from chaenopsid blennies in which the dorsal fin is used for signalling in aggressive male interactions as well as for courtship. Male chaenopsid blennies often have very exaggerated dorsal fin heights. Parac1inins are quite variable for dorsal fin height among species, much less so between sexes. Some species have very shon even dorsal fins, while others have elongate spines at the anterior of the fin (Figure 10, Chapter 2). The particular dimorphism patterns are less interesting than the overall allometries along the c1adogram. Primitively, allometries and dorsal fins are quite low. At node 3, there is quite a large jump in allometry, with a decrease at nodes 2 and 1. The dorsal fins of species above nodes 2 and 1 are not low however, they are among the highest in the clade. Apparently, dorsal fins are growing very quickly in the species at the center of the cladogram relative to primitive species, allowing them to achieve a much higher first ponion of this fin. Species in clade 3, however, do not seem to have increased growth rates to achieve their high dorsals. The 119 PosterIor Body 6 characters ~ 6r------.c a. L. o. _.EL.4 "'1; _0 oL. o L..c 2 ·0 ~ E :::I Z 0 T-,-up~~~~~~~~~~~~~~~+_~_Bij CJ) =:l CJ) E CJ) CJ) CJ) ra CJ) =:l 'E Cii CD CJ) CJ) 'c .c C> .c "0 'E CJ) =:l 'c 0 'c =:l c:: c:: iU CD .~ CD ra =:l c:: CJ) .c 0 c:: iU '0.. .~ ra ttl c:: c. E 'iii .~ 0 'm 0 'C Q) Cii .D C> c:: 15 0 ~ :§- s C> ~ E >. 0 Q) c:: .... c:: C> '0 'x CD 0 c:: ttl C, $ CJ) CD ::c: c:: ttl CD ~ c:: Cii Q) -= '0 .£: ~ E ~ .D i!! .£: c:: E X U5 C> 'c == Figure 48. Summary of dimorphism in posterior body measures. Left column = males relatively larger, right column = females relatively larger. 120 divergence dimorphism ; .~ ; .. .. g ] ·s .0; ~ d i!" ! f: .." .a. E " " ~ ... :;; " .~ :; ::! e ] ~ 11 " " § ~ " :~ } :; .~ ... :a i " ~ B S ~ c :9 " .:!! e l ~ ~ ~ t ~ i " ~ I ~ 0.94 r:I 0.82 1 0.94 ',----- 2 ~ 0.98 r:I 0.87 1 0.95 ',------3 ~ 1.12 r:I 0.94 , , 1 1.06 ,------4 <; 1.02 r:I 0.87 FIRST DORSAL SPINE (7 • 18) 1 1.04 divergence dimorphism .. :0 .~ .~ ; . .0; .. 3 .~ ~ e .~" i5 :5 l! :5 .z .. f: ~ " ~ 3 ... .~ ~ .g" " ] :! ·iii e ~ ~" ~ ~ j :a .;;i5 8. -e '0; ~ ~ .:!! 8 ~ ::J '" 1 t .. J: ~ ~ .s .z 6 18 ~ I ~ 0.96 cf 0.97 1 0.96 ',----- 2 S! 1.02 cf 0.98 1 0.97 ',------3 ~ 1.07 cf 1.04 " 1.12 ,------4 ~ 0.98 cf 0.96 SECOND DORSALSPINE (12-19) 1.10 Figure 49. Dimorphism, divergence, and mean allometric coefficients for two dorsal spine characters. 121 difference must occur earlier in their life history. This can be seen in Figure 50, which shows infrons, naeorhegmis, marmoratus, alrivelis, and asper (all members of clade 3) have the highest intercepts, and therefore end up with elongate first dorsal spines without having high allometries during juvenile and adult growth. Species with the lowest dorsal fins, integripinnis, cingularus, grandicomis, walkeri, and nigripinnis all have low intercepts. Species with elevated allometries are sandwiched between the low-finned and high-finned species. Even with higher allometries these species never quite catch up in fin height to those species with initial high intercept values. Clearly some important shape changes within clade 3 occur before the juvenile stage. Figures 44 and 51 show there is no particular trend toward increasing or decreasing dimorphism within the median fins. Either males or females may be dimorphic for any of these characters, there is no clear pattern favoring exaggeration of these traits in either sex. Total dimorphism A summary of all dimorphiC characters shows a relatively equal division between males and females for relatively larger traits (Figure 52). Scaled dimorphism indices, shown in Figure 44, show the most primitive species have by far the most divergent adults, with more derived species fluctuating up and down. Although amount of dimorphism seems similar in asper and monophthalmus, for example, qualitatively it is quite different. Paraclinus asper along with its two closest relatives has reversed the dimorphism present in monophthalmus so its females may be relatively larger for a trait that is exaggerated in males of the remainder of the paraclinins. Within the clade, dimorphism is decreasing and reversing. Very few characters are similarly dimorphic between clades 3 and 1. These modifications have been accomplished by neoteny, acceleration, and pre- or post-displacement. These changes are independent of and do not reflect the ontogenetiC paths producing dimorphism within a species. 122 Length of dor.a! .pine # 1 -.....CO, Clad. 8 -l'- .. ····Cl.d. 1 &: P. """,IIINa P. '~IIM"oe",c.. P. ",.no.,.... Lenlth of dor.. l .pin. #2 .. ' Clad. 8 -.....~ I N..... - Clade 1 It P. d,.."'I1'''' P. .rll"dCc:owa.c.. General Size Figure 50. Slope and intercept differences for growth of the first two dorsal spines in different paraclinin lineages. 123 W.dlan FIns 8 characters (/) :l If) E (/) en en en (1S ro en :l :l "E Q) If) "E .r:. C) .r:. "E en :l "E (/) "C :l c: If) Cii Q) .1:: Q) ro 0 "E ::l c: c: 1il ::l ... u c: (tj "0. ";:: (1S "~ (/) 0 .r:. 0. "iii c: ~ E "w ";:: Q) (tj r5 C) Q) c: Cii 0 ~ '0 "0. "S C) .c Q) E 0 0 ~ E >. 0 .c ... Q) c: c: ";:: C) "0 "x CD 0. ~ .... c: If) Q) ~ c: "E ctl 0 Q) cu ctl C) c: ~ (1S CD ~ (/) ctl ctl ctl .c E c: E X en c, "E "0 "~ ;: .E E ~ .c ~ "w co £ Figure 51. Number of sexually dimorphic median fin characters in Paraclmus" Left column = males relatively larger, right column = females relatively larger" 124 Totcl DImorphIsm o ~ ~ 16 ..o ~ ~12 -0- _0 o -a 8 Loa.. ID~ ~ 0 4 E :;, Z 0 U) :J U) E U) U) ctl U) U) a; til :J "E Q) fJ) fJ) "c ..c: .a Ol ..c: "E U) :J "c U) "0 :J c: E Q) .1:: Q) ctl 0 "c :J c c cu :J u c: "5. ";:: nl nl "(j) c: "~ fJ) 0 ..c: a. E "iii cu ";:: u ...... 0 '5 "5. "3 Q) cu Ol Q) Q) c: cu E 0 0 Ol ~ E .D 0 .D .... c: ~ c: ";:: Ol "0 "x Q) >- .... Q) c: U) ~ c: a. .... ctl 0 Q) Ol c: S III Q) °E ~ til nl nl .s E co a; .D E c: E X en Ol °c "0 oE: :: ~ E ~ .D ~ °iii nl ~ Figure 52 Total number of sexually dimorphic characters in Parclinuso Left column = males relativly larger, right column = females relatively largero 125 Shape differences among species Principal component analysis of morphometric data for all species together gives shape axes, PC2 and 3 (Figure 53). The first principal component is a size axis, with all character loadings high and positive. Vector correlations for the characters contributing most to the data spread in the space defined by PC2 and 3 are plotted. Clade 3 species separate well from the remainder, with only a bit of overlap with some species. Clade 11ies closest in space to cingulatus and grandicomis, while clade 2 lies between these groups, though it is closest to clade 3. SpeCies not asSigned to any particular clade are shown enclosed in a pOlygon, and they are largely mixed within this space. Clade 3 is characterized by a larger interspace between dorsal spines 3 and 4 (character 13-14), and by longer first dorsal spines (characters 7-18, 12-19). More primitive species have longer and wider jaws (characters 1-10,9-11), wider spacing between dorsal spines 1 and 2 (character 7-12), and between dorsal spines 2 and 3 (character 12-13). The remainder of the species are intermediate for these characters. Most of the characters which contribute to group separation are dimorphiC for some species; perhaps sexual selection for extremes in these characters is driving speciation, or perhaps simply causing morphological change once speciation has occurred. The dimorphism is spread throughout different clades, so it does not appear to be a simple causal relationship. Within species discriminate analysis The results of discriminate analyses of shape for species with large sample sizes are shown in Figures 54 and 55. Table 10 contains the character correlations for those species not discussed in Chapter 1. The distances among groups and the widths of within-group distributions give some indication of among-group variability. The species for which males, females, and juveniles are very different in shape show narrow distributions (on the horizontal axis) and 126 . •• , , • emalD.1q .pealei·. '.. . ." . " ...... " '...... - . '. PC25% 0.1 (13-14) vector correlations of characters with axes -o.s o.s (12-13) (7-18) -0.5 Figure 53. peA of Paraclinus species. Polygons enclose indicated groups, vector correlations show which characters contribute to data scatter. 127 E:ze'T'pss a.sper Paracli72'US i72jrons .. - UI - DF 1 96% DF 1 98.5% Paraclill:u.s monophthalmus Para.clinus mcmophthaZmu.s rl-r21 r22-r42 DF 1 90% DF 1 88% ParacLin"Us marmoratus Parae linus beebei M n=15 DF 1 99.5% DF 1 99.5% Figure 54. Size-free discriminate analysis of males, females, and juveniles within each of five species. Percent refers to the amount of variance accounted for by each axis. M = males, F = females, J = juveniles. Sample sizes prevented analysis of all characters in monophthalmus, so two analyses were performed. Sample sizes are indicated next to pOlygons enclosing groups. 128 Parae lin'US cingu.latus Paraelin'US cingu.latu.s rl-r25 r26-r42 DF 1 94.8% DF 1 92% PaTaelinu.s walkeri Pa.ra.clinus integripinnis ~ -o DF 1 99.1% DF 1 98.9% Figure 55. Size·free discriminate analysis of males, females, and juveniles within each of three species. Percent refers to the amount of variance accounted for by each axis. M = males, F = females, J = juveniles. Sample sizes prevented analysiS of all characters in cmgulatus, so two analyses were performed. Sample sizes are indicated next to pOlygons enclOSing groups. 129 Table 10. Character correlations with the first discriminate function. Analyses based on size-free data resulting from regression. Abbreviations follow Table 9; values for P. sini, !ascialus. mericanus, and nigTipinnis are all found in Table 1, Chapter 1. Negative values indicate female relatively larger, positive indicate male relatively larger. c t w z h p r x i Head 1-7 0.75 0.25 -0.32 -0.36 1-8 0.67 0.32 0.38 0.36 0.56 0.34 1-6 0.62 0.64 -0.40 7-6 0.57 2-6 0.57 7-8 0.34 0.25 0.50 0.34 1-2 0.45 2-4 0.67 0.36 0.35 0.46 0.41 4-5 0.27 -0.48 5-5' 4-4' 0.42 0.31 -0.31 0.29 3-3' 0.78 0.44 0.44 0.50 2-2' 0.47 0.38 0.43 Ja,,' 1-10 0.82 0.54 0.48 0.72 0.70 0.50 0.25 9-11 0.64 0.71 0.61 0.44 0.64 0.33 -0.23 Midbody -0.26 7-12 -0.28 0.41 12-13 0.30 -0.35 13-14 -0.32 14-15 -0.50 -0.31 -0.29 15-16 -0.50 0.21 -0.37 -0.25 -0.32 8-17 -0.63 -0.43 -0.34 -0.51 -0.71 -0.62 -0.30 7-17 -0.68 -0.40 -0.30 -0.71 -0.47 -0.57 8-16 -0.57 0.35 -0.59 -0.30 -0.61 16-17 -0.55 -0.34 0.31 0.45 0.43 1.30 Table 10. continued c t w z h p r x i Post-body 16-30 0.34 30-31 0.38 31-32 0.31 0.40 0.34 0.51 0.31 0.53 32-17 0.41 16-31 0.47 17-30 0.34 0.36 0.64 0.49 0.64 Median Fins 7-18 -0.33 0.25 -0.33 12-19 0.33 13-20 0.49 0.23 14-22 -0.37 -0.38 0.53 15-23 0.31 0.44 32-33 0.56 0.36 0.32 17-34 0.45 0.30 0.35 0.44 Length 0.34 0.33 -0.29 -0.29 1-35 131 greater group separation. For example, males, females, and juveniles of beebei and marmoratus are shaped much more differently than the same groups in monophthalmus and infrons. Juveniles are always located in morphospace ber;;.;en mal~ and females, but most often lie closer to males. This means that overall, females diverge more from juvenile shape than do males, as discussed in Chapter 1, and this holds true for most species. In infrons, however, juveniles more closely resemble females, and several species seem to have juveniles equidistant from both adult morphologies (asper and beebei). These species then have females diverging relatively less or an equal amount than males from the juvenile morphology. Characters contributing to group separation, those which are highly correlated with the first discriminate axis, are scattered throughout the body regions and are important to different extents in different species. They also tend to be characters that are sexually dimorphic. Some species which are vexy different in dimorphism (clade 3 members) also are those in which dimorphism is reversed from the primitive type. It is quite interesting that in the most dimorphic species, males and juveniles have the most similar shapes, while in the least dimorphic species, females and juveniles have the most similar shapes. Multivariate analvsis of allometries PCA of male, female, and juvenile allometric coefficients shows male, female, and juvenile growth are more similar within these groupings than within phylogenetic groupings (Figure 56). Groups are enclosed by convex pOlygons and vector correlations with PC1 and PC2 are indicated in the diagram. Group centroids are indicated by upper case letters within the polygons, and are connected to help indicate direction of divergence. Again, higher correlation of a character with an axis indicates the character helps account for variation along that axis. Direction of the vectors in this space indicates the direction of maximum variation for that character. Male and female allometries form adjacent but non-overlapping groups. Juveniles fall All Characters 132 F PC 1 17% 1.0 ~------~ Character correlations with PCI and PC2 0.8 j .... 1.DIUL (2) 0.6 0.4 0.2 0.0 -0.2 -0.4 -0.6 midbod, (3) -0.8 -1.0 -1.0-0.8-0.6-0.4-0.2 0.0 0.2 0.4 O.S 0.8 1.0 Figure 56. Results of PCA on allometric coefficients. All characters were included. Polygons enclose males, females, and juveniles. Group centroids are represented by M, F, or J. 133 between these two groups, overlapping both. Adult allometries diverge from juvenile aHometries in the same way for males of all species and for females of all species. Males diverge from juveniles by increased growth in head characters, while females diverge primarily in terms of increased growth in midbody characters. Although posterior body and dorsa~-fin characters are also highly correlated with PC1 and PC2, they contribute to scatter at right angles to the direction providing most group separation. Juveniles of all species are growing in apprOximately the same way, though their starting shapes, the result of larval allometries, are quite different. This indicates that the larval allometries must also be qUite different from juvenile and adult allometries, as seen by Strauss (1992) in Poeciliids. These patterns may be better understood by analyzing allometries by body region. The results of a separate analysiS of head allometries is shown in Figure 57. Most head measures show increased allometry in adults relative to juveniles, with males and females diverging for different characters. Females are increasing primarily in character 4-5, and 5-5'. These are distance from preopercle to opercular spine and head width at the opercular spine, respectively. Males show increased growth in jaw measures, some head length and width measures. Although there is a general trend of separate divergence pathS, males and females overlap to a greater extent than they when all characters were considered. It seems reasonable to expect, if head shapes are quite different in different clades, that analysis of head allometries would show separation of lineages similar to that seen with the sexes. However, this does not occur when all sexes are analyzed together (Figure 58). There is considerable overlap among clades 1, 2, and 3. When males, females, and juveniles are analyzed separately there is separation along lineages (Figure 58). Relationships among these groups are not maintained in the separate analyses, so that for all females, clades 1 and 2 are the most different, while in males and juveniles clades 1 and 2 are closest along the first axis, which accounts for a greater proportion of the variation. Related groups of females are more similar Head Characters 134 J PC 1 32% 1.0 ~------~ width. depth 0.8 (7-1S); ("-4') 0.6 0.4- preoperele to oparel. (4-~) 0.2 0.0 Jaw 1."9th -0.2 ....Idth -0.4- -0.6 -0.8 Character correlations with PCl and PC2 -1.0 +---~----~--~--~----~---+----+---~--~~--~ -1.0 -0.8 -0.6 -0.4- -0.2 0.0 0.2 0.4- 0.6 0.8 , .0 Figure 57. Results of PCA on allometric coefficients for just the head region. Polygons enclose males, females, or juveniles. Group centroids are represented by M, F, or J. 135 Head characters Females Kales ., Clad. 1 ~ en \ a • n &0 ·f (\2 eC J t~lad. 1 X em Z ef '~2 .C Y h b PC 1 PC 1 25% Juveniles All Groups t s • f f~·P en (\2 <:.~ -"... , o Il. 2 ·C em em Z . 1- C C e PC 1 32% PC 1 32% Figure 58. Results of PCA on head region allometries (as in Figure 57) with clades enclosed by pOlygons (bottom right). Both top figures and the bottom left represent PCAs of females, males, and juveniles separately. 136 for allometry of head length, while jaw size and head width separate lineages of males. Juveniles do not mirror either adult group, with all head allometries rather than subgroups contributing to lineage separation. Allometries of body characters considered together showed less overall divergence from juvenile allometries, and males overlap juveniles to a greater extent than do females (Figure 59). Males of several species- mexicanus, barbatus, marmoratus, integripinnis, and tanygnathus- are almost superimposed on their juvenile values. Females in general diverge from juveniles in the direction of higher values for midbody characters, while males diverge in the direction of lower values for posterior body and midbody characters. Males also increase growth rate of body depth measures (character 7-8). Juveniles have higher allometries for posterior length and depth as well as some midbody lengths than adults. This complements the lower values for growth in the head region, resulting in proportional changes of head to body size seen in adults. Analyses of males, females, and juveniles separately show markedly less difference among lineages for males and juveniles than for females (Figure 60). Within juveniles, clade 1 separates from clades 2 and 3 based mostly on characters contributing to overall length relative to depth. Male lineages overlap almost completely, while there is good separation of female lineages. Characters contributing 10 separation along PC1 (for females) are mostly components of length. Dorsal fin allometric coefficients were unique in shOwing phyletiC grouping when all sexes were analyzed together (Figure 62). Conversely, there is no grouping of males, females and juveniles as had been the case for the other body regions (Figure 61). Juveniles tend to have higher allometries for most dorsal spine lengths, but there is a lot of overlap. The different clades, however, separate out quite well. Characters contributing most to the phyletic separation are allometries affecting spacing of the first five dorsal spines. Females are less variable within lineages than are males and juveniles, they are more tightly clumped within groups, perhaps indicating more conservative allometric patterns or perhaps convergence within lineages to ... - ----.------137 Body characterll PC 1 34% 1.0 .------~~~~~~------Midbody depth/lenllth (8-1 (7-17) O.B 0.6 0.4 0.2 Body depth (7-8) 0.0 -0.2 -0.4 «(30-31) -0.6 -0.8 Character correlations with PCl and PC2 -1.0 +---+----;----+----+---;---+----+---1--+---1 -1.0 -0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0 Figure 59. Results of PCA on body character allometries. Polygons enclose males, females, and juveniles. Group centroids are represented by M, F, or J and are connected. 138 Body Characters Females Kales h Clad. t-e CD ~ C\l .-4 .n C\l C\l • f C\l 0 c • c.. 0 fl.' y c.. .., ...p ~ • 'hi Clacl. 3 r c· PC 1 39% PC 1 44% Juveniles All groups .c y ~ 10 en • c t-e ~ h LO C\l C\l II C\l Z C\l 0 c..0 • c.. ef • PC 1 33.6% PC 1 34% Figure 60. Results of peA on body region allometries (as in Figure 59) with clades enclosed by polygons (bottom right). Both top figures and the bottom left represent peAs of females, males, and juveniles separately. 139 J ------~ ,I I I F Dorsal fin characters PC 1 29% 1.0 -r------. O.B SpGcln; of dG ....1 .pln.. 2-e 0.6 0.4 (12-11) 0.2 (12-13) 0.0 -0.2 -0.4 (7-12) Spacln; of dOl'llGI .pln.. 1-2 -0.6 (14-22) -0.8 Correlations of characters with PCl and PC2 -1.0 -1.0 -0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 O.B 1.0 Figure 61. Results of peA on dorsal fin character allometries. Polygons enclose males, females, and juveniles. Group centroids are represented by M, F, or J and are connected. 140 Dorsal Fin Characters Females Kales • f OClad. y .c ~r ~n. l'e '1 ,.- ~." co - z .c PC 1 38% PC 1 33% Juveniles z~ All Groups h Clad. 2' y f .c rrl' p • • c • f Clacl.13 f • p •• f • PC 1 30% PC 1 29% Figure 62 Results of PCA on dorsal fin allometries (as in Figure 61) with clades enclosed by polygons (bottom right). Both top figures and the bottom left represent PCAs of females, males, and juveniles separately. 141 similar growth. Interestingly, barbatus, of clade 3, has quite different dorsal spine heights than others of its group, with a low even dorsal fin. Other species in clade 3 have a triangular shape to the dorsal fin, with quite high anterior spines. E,,'en so, allometries for barbatus are similar to other species of clade 3, although adult allometries are more different from those of their juveniles than adults of the other species seem to be. Adults of barbatus also have much higher third and fourth spines than adults of other clade 3 spines, which is caused by higher growth rates in adults of this species. The fact that the group with the most extreme dorsal fin height, clade 3, lies between the more moderate clades in allometries for these characters indicates again that there are probably profound differences in larval allometries. These differences are evident in scatterplots such as shown in Figure 50, where groups of species have quite different intercepts. It would be interesting to see if larval allometries are more conservative phylogenetically than those of juveniles and adults. Strauss (1992) found that for peociliid fishes, allometries of larvae contained more phylogenetic information than those of adults. In this case, juveniles and adults retain phylogenetic information within one subset of the characters, but in general when all classes are considered together phylogenetic information is overwhelmed by differences due to age and sex. That dorsal fin characters show a phyletic component when all groups are analyzed together indicates these growth rates are conservative among sexes; male, female and juvenile growth is behaving similarly within the clades. This may indicate that for dorsal fins selection is acting similarly on males, females, and juveniles, while for the other characters selection is acting differently on the three groups. CONCLUSIONS Ontogeny of sexual dimorphism within the Paraclinini is quite complex, both within and 142 among species. For this group, differential growth in males is not the main cause of adult dimorphism. Rather, allometric shifts in both sexes produce adult shapes with approximately equal frequenc.y. The sex that shifts its allometric growth is not necessarily the sex for which a trait is relatively larger. Character that might be assumed to be under selection for exaggeration in one sex, such as larger male head size, result from neoteny in the other sex (relative to juvenile growth rate) as often as acceleration in the sex for which the larger trait is presumed to be advantageous. Females, rather than being shaped like large juveniles, are actually more different from juveniles in shape than are males. This is largely due to allometric differences in dimorphic characters. On this time scale then, females should be considered the divergent sex. Phylogenetic analysis revealed three main lineages within the clade, the integripinnis walkeri pair, the beebei1ehlmanni-tanygnathus clade, and the asper-infrons-barbatus-marmoratus naeorhegmis group. These groups are likely to remain stable, though positions of some of the other species may change as more data become available. The most primitive species are grandicomis, nigripinnis, and cingulatus. The position of Exerpes asper within the clade indicates that its single species should be included within the genus Paraclinus. Principal component analysis of allometric coefficients among species shows that males and females are divergent from juveniles for growth rates, and that differences across species are overall more similar than allometric differences among clades. Characters accounting for this divergence are primarily head and midbody measures, which are also most often dimorphic within the clade. When sexes are analyzed separately, often a phyletic component of similarity is present. This indicates that in general, males and females must shift allometric growth patterns in different directions, resulting in no clear phyletic pattern when all three groups are considered together. Females cluster more tightly in the rate spaces described by the PCAs than do males or juveniles, indicating they are more conservative in allometric patterns among species. Dorsal-fin allometries are the exception, having a clear phylogenetiC component when males, females, and 143 juveniles are considered together. For these characters, then, all three groups vary in similar ways within their clades. Fairly extreme sexual dimorphism within the Paraclinini seems to be the ancestral condition and has been variously modified within the clade. The trend is toward less extreme male and female differences, with occasional reversal of a dimorphic character. The decrease in amount of dimorphism seems to have occurred primarily through neoteny of the relatively larger sex, acceleration in the relatively smaller sex, and post-displacement of the timing of allometric divergence. Changes in juveniles also have affected amount of dimorphism; for example, neotenous juveniles result in less extreme adults. These evolutionary changes are independent of and in no way reflect the ontogenetic paths producing dimorphism within a species. Thus, presence of sexual dimorphism does not require a particular explanation in any of these individual species. Dimorphism is clearly the ancestral condition in these fish and is to be expected. It is the reduction and reversal of sexual dimorphism in paraclinin blennies that need to be explained. 144 APPENDIX 1 Description of Landmark Points (Figure 2: Chapter 1) 1: anterior tip of nasal bones; 2, 2': interorbital head pore; 3, 3': maximum cheek width (not a landmark); 4, 4': most posterior edge of the preopercle; 5, 5': tip of opercular spine; 6: lateral projection of 5; 7: insertion of 1st dorsal spine; 8: anterior insertion of pelvic fins; 9: greatest posteriodorsal expansion of maxilla; 10: posterior tip of maxilla; 11: greatest posterioventral expansion of maxilla; 12: insertion of 2nd dorsal spine; 13: insertion of 3rd dorsal spine; 14: insertion of 4th dorsal spine; 15: insertion of 5th dorsal spine; 16: insertion of 10th dorsal spine; 17: insertion of 1st anal spine; 18: tip of 1st dorsal spine; 19: tip of 2nd dorsal spine; 20: tip of the third dorsal spine; 21: attachment of dorsal fin membrane to 4th dorsal spine; 22: tip of 4th dorsal spine; 23: tip of 5th dorsal spine; 24: origin of most dorsal pectoral ray; 25: tip of most dorsal pectoral ray; 26: origin of 8th pectoral ray; 27: tip of 8th pectoral ray; 28: origin of most ventral pectoral ray; 29: tip of most ventral pectoral ray; 30: posterior edge of hypural plate, dorsal surface; 31: posterior edge of hypural plate, ventral surface; 32: insertion of 2nd anal spine; 33: tip of 2nd anal spine; 34: tip of 1st anal spine; 35: posterior midpoint of hypural plate. 145 REFERENCES Alberch, P., S. 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