Do constructional constraints influence cyprinid
(Cyprinidae: Leuciscinae) craniofacial coevolution?
C. DARRIN HULSEY* and PHILLIP R. HOLLINGSWORTH JR
Department of Ecology and Evolutionary Biology University of Tennessee, 569 Dabney Hall
Knoxville, TN 37996, USA
Received 19 August 2010; revised 8 December 2010; accepted for publication 8 December 2010
Constraints on form may determine how organisms diversify. As a result of competition for the limited space within
the body, investment in adjacent structures could represent an evolutionary compromise. For example, evolutionary
trade-offs resulting from limited space in the head could have influenced how the sizes of the jaw muscle, as well
as the eyes, evolved in North American cyprinid fishes. To test the evolutionary independence of the size of these
structures, we measured the mass of the three major adductor mandibulae muscles and determined the eye volume
in 36 cyprinid species. Using a novel phylogeny, we tested the hypotheses that the sizes of these four structures
were negatively correlated with each other during cyprinid evolution. We found that evolutionary change in the
adductor mandibulae muscles was generally positively and/or not correlated, suggesting that competition for space
among cyprinid jaw muscles has not influenced their evolution. However, there was a negative relationship
between mass of adductor mandibulae 1 and eye volume, indicating that change in these physically adjacent
structures is consistent with an evolutionary constructional constraint. © 2011 The Linnean Society of London,
Biological Journal of the Linnean Society, 2011, 103, 136–146.
ADDITIONAL KEYWORDS: ecomorphology – freshwater fish – integration – modularity – North America –
phylogenetic comparative method.
INTRODUCTION
For many morphological phenotypes, allocation to one
structure may compromise investment in another
structure. These trade-offs operate at many levels of
biological organization and among diverse com-
ponents of organismal design (Garamszegi, Moller &
Erritzoe, 2002; Striedter & Northcutt, 2006). From
a developmental perspective, if extensive somatic
investment is made in one structure, this could limit
soma dedicated to the formation of another structure
(Emlen, 2001; Moczek & Nijhout, 2004). It is also
possible that constructional trade-offs constrain
investment in phenotypes because the structural
space in organisms is limiting (Barel, 1983; Herrel,
Aerts & De Vree, 2000; Devaere et al., 2006). If one
structure is enlarged, then it could limit the size
of other structures, especially adjacent ones. For
example, debate continues regarding the modular
versus compensatory evolution of mammalian brains
(Barton & Harvey, 2000; de Winter & Oxnard, 2001).
Similarly, a recent study of the craniofacial morphol-
ogy of cichlid fishes found little evidence to bolster the
frequently cited idea that craniofacial constructional
constraints were evolutionarily important in teleost
fish (Hulsey, Mims & Streelman, 2007). However, the
absence of constructional constraints in this unique
cichlid lineage might not generally characterize diver-
sification in other diverse groups such as cyprinid
fishes. To examine a set of long postulated con-
structional constraints, we quantified morphology,
reconstructed a novel phylogeny, and then employed
independent contrasts to examine whether there are
any negative correlations among adductor mandibu-
lae (AM) muscle masses and/or eye volume in North
American cyprinid fishes.
Cyprinid fishes represent one of the most species
rich groups of teleosts (Strange & Mayden, 2009). In
species-rich lineages, identifying what components of *Corresponding author. E-mail: chulsey@utk.edu
Biological Journal of the Linnean Society, 2011, 103, 136–146. With 3 figures
© 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103, 136–146 136
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