Download Ze`ev Bernstein1, Shivani Sundaram2, Vikram B. Baliga3, and Rita S

Assessing the Convergence of Feeding Kinematics in Labrid Cleaner Fishes
Ze’ev
1
Bernstein ,
Shivani
2
Sundaram ,
Vikram B.
3
Baliga ,
and Rita S.
3
Mehta
1: Pacific Collegiate School 2: Monta Vista High School 3: Department of Ecology & Evolutionary Biology, Long Marine Lab, University of California, Santa Cruz
Abstract
Among fishes, cleaning behavior is a mutualistic relationship wherein a
cleaner species will consume ectoparasites and dead skin from the body
of other taxa. This behavior has evolved numerous times in the marine
teleost family Labridae (wrasses, parrotfishes, and weed whitings). While
the functional morphology of feeding in some labrid cleaners has been
examined, the mechanism by which these fishes remove ectoparasites
from their host is not clearly understood. The purpose of the study is to
analyze the biomechanics of the skulls of cleaner fishes and determine
whether they exhibit evolutionary convergence, which is when distantlyrelated taxa evolve similar traits due to similar ecology. We obtained 10
cleaner and 11 non-cleaner species of the Labridae family and filmed
lateral feeding sequences at 1000 frames/second with a high-speed
camera. Afterwards, we digitally plotted landmarks on the skull and
determined the displacement and timing variables of the fishes’ gape,
premaxillary protrusion, lower jaw angle, and cranial elevation. After data
collection, we used Principal Components Analysis to analyze the data
variability across all species. This size-corrected kinematic analysis
revealed that cleaners display short and rapid jaw protrusions and
cranial movements. We determined that the cleaner fish display 17.78%
convergence with a P-value (0.007) below the index of significance
(P<0.05). Therefore, we concluded that when placed in a phylogenetic
comparative context, labrid cleaner fish exhibit higher evolutionary
convergence than would be expected by chance.
Methods (continued)
Figure 2. Landmarks used during kinematic analysis.
Displays 6 landmarks: 1) the anterior tip of the premaxilla,
2) the posterior margin of the nasal bone, 3) the
approximate point of the articulation between the
hyomandibula and the neurocranium, 4) the dorsal margin
of the insertion of the pelvic fin (a reference point), 5) the
approximate articulation of the lower jaw with the
quadrate, and 6) the anterior tip of the dentary.
Objective
To understand the extent to which kinematic traits are similar among cleaner
species, considering the extensive ecological and biomechanical diversity of
feeding behaviors among the labrid family.
From
Stayton (2015)
• Digitized sequences using
Tracker to monitor 6 external
landmarks (see Figure 2).
• Measurement of
displacement (mm) and
angular variables (degrees)
accompanied by timing
variables (ms): time to peak
gape, time to peak
premaxillary protrusion, time
to peak lower jaw rotation,
time to peak cranial
elevation, time to full jaw
retraction (see Figure 3).
• Size-corrected phylogenetic
principal components
analysis (pPCA; Revell 2009)
using 9 kinematic variables
in R to generate phylokinematic spaces.
• Quantification of evolutionary
convergence and
significance following Stayton
(2015).
Figure 3. Distance and angular variables used during
kinematic analysis.
Results
Methods
• Measured the standard lengths of 1-7 juvenile individuals for 21 labrid
species, of which 10 are known to exhibit cleaning behavior.
• Acquired through the aquarium trade.
• Filmed lateral feeding sequences at 1000 frames per second in 1024 x
1024 pixels.
Choerodon fasciatus
Bodianus bimaculatus
Bodianus rufus
Pseudocheilinus hexataenia
Pseudocheilinus evanidus
Coris gaimard
Thalassoma jansenii
Thalassoma hardwicke
Thalassoma lutescens
Thalassoma duperrey
Gomphosus varius
Hemigymnus melapterus
Larabicus quadrilineatus
Labroides pectoralis
Labroides dimidiatus
Diproctacanthus xanthu rus
Pseudojuloides cerasinus
Halichoeres garnoti
Halichoeres cyanocephalus
Halichoeres bivittatus
Anampses neoguinaicus
0
PP(state=1)
length=31.042
Cf
Figure 5. Calculation of the similarity-based measures of convergence. Note:
Adapted from Stayton (2015). Large circles represent tips, small circles represent
ancestral nodes, and lines represent lineages between ancestors and descendants.
Two tips—Tip 1 and Tip 2—are being assessed for convergence. C1 = 1 − (Dtip/Dmax).
Conclusions
• A C1 value of 0.1778 indicates 17.78% convergence between cleaner
species.
• A P-value of 0.007 indicates that only 0.7% of the simulation results were
higher than our convergence index.
• We found significant kinematic convergence among labrid cleaner fishes.
• These trends in kinematic movement may be driven by selection
pressures to promote low displacement, rapid movement.
Future Work
• Morphological differences in the shape of the premaxilla and muscle
recruitment patterns
• Cleaning over ontogeny
References
Baliga, V. B., & Law C. J. (2016). Cleaners among wrasses: Phylogenetics and evolutionary patterns of cleaning behavior within
Labridae. Molecular Phylogenetics and Evolution. 94A, 424-435.
Baliga, V. B., & Mehta R. S. (2015). Linking Cranial Morphology to Prey Capture Kinematics in Three Cleaner Wrasses: Labroides
dimidiatus, Larabicus quadrilineatus, and Thalassoma lutescens. Journal of Morphology. 276, 1377-1390.
Bb
Brown, Douglas. Tracker Video Analysis and Modeling Tool. Vers. 4.94. Computer software. 2009. Java (JRE) 1.6. 20 Sep. 2016
Côté, I. M. (2000). Evolution and ecology of cleaning symbioses in the Sea. Oceanography and Marine Biology. 38, 311-355.
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Felsenstein, J. (1985). Phylogenies and the Comparative Method. The American Naturalist. 125, 1-15.
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Powell, V., & Lehe, L. (n.d.). Principal Component Analysis. Retrieved August 2, 2016, from http://setosa.io/ev/principalcomponent
- analysis/
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Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution. 63, 3258-3268.
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Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217223.
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Stayton, C. T. (2015). The definition, recognition, and interpretation of convergent evolution, and two new measures for
quantifying and
assessing the significance of convergence. Evolution. 69, 2140-2153.
Wainwright, P. C., Bellwood, D. R., Westneat, M. W., Grubich, J. R. and Hoey, A. S. (2004). A functional morphospace for the skull
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Acknowledgments
1
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Figure 1. Evolutionary relationships between the 21 taxa and identification of cleaners from
Baliga and Law (2016). Red gradient represents the Bayesian posterior probability (PP) of
cleaning behavior along each branch of the tree. The length of the scale is in millions of
years.
Figure 4. Primary axes of kinematic variation. Cleaning behavior is represented in red.
Variables that correlated most strongly with the PC axes are represented by arrows that
indicate the direction in which the variables increase. Cleaner species seem to display rapid
and short jaw movements, especially in terms of cranial elevation, premaxillary protrusion,
and jaw retraction.
We would like to Chris Law for helping us with data analysis, and Jacob Harrison for assisting us with data collection and
offering helpful discussion. We thank Holly Hermann-Sorensen for assistance in filming animals. Additionally, we would
like to thank our parents for supporting us.
Author Contact Information:
[email protected] and
[email protected]