Hybridization produces novelty when the mapping of form to function is many to one
© Parnell et al; licensee BioMed Central Ltd. 2008
Received: 04 January 2008
Accepted: 28 April 2008
Published: 28 April 2008
Evolutionary biologists want to explain the origin of novel features and functions. Two recent but separate lines of research address this question. The first describes one possible outcome of hybridization, called transgressive segregation, where hybrid offspring exhibit trait distributions outside of the parental range. The second considers the explicit mapping of form to function and illustrates manifold paths to similar function (called many to one mapping, MTOM) when the relationship between the two is complex. Under this scenario, functional novelty may be a product of the number of ways to elicit a functional outcome (i.e., the degree of MTOM). We fuse these research themes by considering the influence of MTOM on the production of transgressive jaw biomechanics in simulated hybrids between Lake Malawi cichlid species.
We characterized the component links and functional output (kinematic transmission, KT) of the 4-bar mechanism in the oral jaws of Lake Malawi cichlids. We demonstrated that the input and output links, the length of the lower jaw and the length of the maxilla respectively, have consistent but opposing relationships with KT. Based on these data, we predicted scenarios in which species with different morphologies but similar KT (MTOM species) would produce transgressive function in hybrids. We used a simple but realistic genetic model to show that transgressive function is a likely outcome of hybridization among Malawi species exhibiting MTOM. Notably, F2 hybrids are transgressive for function (KT), but not the component links that contribute to function. In our model, transgression is a consequence of recombination and assortment among alleles specifying the lengths of the lower jaw and maxilla.
We have described a general and likely pervasive mechanism that generates functional novelty. Simulations of hybrid offspring among Lake Malawi cichlids exhibiting MTOM produce transgressive function in the majority of cases, and at appreciable frequency. Functional transgression (i) is a product of recombination and assortment between alleles controlling the lengths of the lower jaw and the maxilla, (ii) occurs in the absence of transgressive morphology, and (iii) can be predicted from the morphology of parents. Our genetic model can be tested by breeding Malawi cichlid hybrids in the laboratory and examining the resulting range of forms and functions.
Biologists are captivated by the evolution of new forms and functions . Over large evolutionary scales, new traits like oxygen metabolism , flowers , limbs  and the vertebrate neural crest  have facilitated the ecological and numerical dominance of the lineages that possess them. On more recent timescales, organisms adapt to their environments by continued innovation and modification of these features. A growing literature seeks to explain the genetic and developmental mechanisms of both macro- and micro-evolutionary novelty .
Two recent but largely separate lines of research address the question. The first amounts to a renaissance in our understanding of the evolutionary role of hybridization [7, 8]. Hybrid organisms are generally unfit when compared to parent populations . However, hybrids may have greater fitness than their parents in extreme environments , when environments fluctuate , or after environmental and/or human disturbance . Hybridization contributes to 'creative' evolution in two major ways: by (i) providing hybridizing species with genetic variation for adaptive traits, or (ii) producing new species. Hybrid origin (or hybrid swarm) theories of evolutionary radiation combine these two ideas [13, 14]. As an example of (i), Grant et al.  used long-term study of Darwin's finches to show that directional introgression of alleles from Geospiza fortis to G. scandens, coupled with natural selection, could explain trends in beak shape and body size. The work of Rieseberg and colleagues on Helianthus sunflowers provides one of the best examples of (ii). Hybrid speciation in Helianthus is a product of chromosomal rearrangement  and ecological selection acting on pleiotropic genes in remote habitats . Helianthus hybrid species specialize in extreme environments, where they out-compete their parents . This phenomenon of transgressive segregation (TS), in which hybrids outperform parental forms, is more common than once believed. Rieseberg and others  summarized data from 1229 traits in 171 experiments and found that 91% of studies reported at least one transgressive trait and that 44% of traits were transgressive overall.
Importantly, Rieseberg et al.  also considered the genetic architecture of TS and proposed that complementary action of genes with additive effects was the major cause. Complementary gene action works as follows (see also Table 1 of ): species A (large) segregates 6 quantitative trait loci (QTL) for size and 4 of these contribute phenotypic effects of 'large,' while 2 contribute phenotypic effects of 'small;' species B (small) also segregates 6 QTL for size, 4 of which contribute phenotypic effects of 'small,' while 2 contribute phenotypic effects of 'large.' Species A and B produce hybrids that intercross to produce F2; after recombination and independent assortment, some F2 are larger than parent A (e.g., F2 with 6 'large' QTL) and some are smaller than parent B (e.g., those with 6 'small' QTL). Thus, complementary gene action may be a general genetic mechanism of TS.
An upshot of this reasoning was that traits experiencing a history of strong directional selection were less likely to exhibit TS . This was codified in Orr's QTL sign test , which compares the distribution of direction of QTL effects to a random expectation, as a quantitative genetic metric of directional selection. Albertson and Kocher  extended this logic to argue that directional selection and genetic architecture limit the evolutionary role of TS. Using Malawi cichlid hybrids, they showed that lower jaw shape, a trait under strong directional selection , did not exhibit TS while the shape of the neurocranium, a trait not under directional selection, did. They concluded that natural selection might constrain the degree of diversification that can be achieved via hybridization. This might hold, in particular, for aspects of the craniofacial skeleton involved in feeding, including the shape of skeletal components, the dentition, and simple levers involved in jaw function [22–24].
We reasoned that MTOM of form to function might contribute to functional transgression in hybrid offspring. Just as complementary gene action describes hybrid trait transgression as the piling up of QTL of the same direction (e.g., 'large') from different parental genomes, we envisioned scenarios in which MTOM parental species might segregate 4-bar links to hybrids in combinations producing biomechanical output (KT) well beyond the parental range. To evaluate this possibility, we characterized the 4-bar mechanism in Lake Malawi cichlids and simulated hybrids using a simple but realistic genetic model. Lake Malawi cichlids are apposite study organisms for this question. They exhibit tremendous morphological diversity on a background of genomic mosaicism [[29, 30], Loh et al. 2008 in review]. Species hybridize in the wild [31–33] and speculation persists that hybridization has contributed to the adaptive radiation of this species flock . Our simulations demonstrate that transgressive function is a likely outcome of hybridization among Malawi species exhibiting MTOM. Functional transgression is a product of recombination and assortment between alleles controlling the lengths of the lower jaw and the maxilla, occurs in the absence of transgressive morphology, and can be predicted from the morphology of parents.
Results and Discussion
Diversity and correlation in the Malawi 4-bar linkage
Correlations (r2) between links and KT among Lake Malawi cichlids are similar for uncorrected (below the diagonal) and phylogenetically independent contrasts (above the diagonal).
We next asked whether correlations among links and KT were robust to the pattern of Malawi cichlid evolutionary history. It has been known for some time that trait correlations should be corrected for phylogeny because related individuals do not represent independent statistical samples . This is a particularly important and difficult problem in the Malawi cichlid assemblage where species are young (e.g., 1000 years, ) and phylogenetic resolution is limited [30, 37]. Table 1 (above the diagonal) shows evolutionarily independent correlations calculated using the phylogenetic topology shown in Additional file 3, employing an approach described in Hulsey et al. . We use a single mitochondrial genealogy because the locus offers more resolution than nuclear genes in this rapidly evolving lineage [30, 37]. The corrected correlations are similar to the uncorrected in all but one case. The lower jaw link, positively associated with KT using uncorrected data, is not associated with KT across the Malawi phylogeny. Further inspection of the data suggests that this is due to lack of power to detect a phylogenetic association (i.e., lack of divergent independent contrasts) as most rock-dwelling mbuna have relatively short lower jaws compared to most non-mbuna taxa.
Comparison of species' trait values (corrected for body size) identified numerous cases of convergence in KT via divergence in link length, or MTOM of form to function . The correlations noted above help to explain this observation. For example, both Cynotilapia afra and Pseudotropheus elongatus have KT values of approximately 0.7, but they exhibit distinct morphologies. Cynotilapia afra has relatively long input and output links, while P. elongatus has relatively short elements of each. We reasoned that hybridization between species like these that are MTOM for function might produce F2 hybrids with extreme KT values, if independent assortment recombines the long lower jaw of C. afra with the short maxilla of P. elongatus (high KT) or the long maxilla of C. afra with the short lower jaw of P. elongatus (low KT). We tested the generality of this prediction using a simple, but realistic genetic model.
Simulated hybrids of MTOM species are transgressive in function
Our Mendelian genetic model assumes no evolution and no environmental variance (VE = 0). We specified that size-standardized lengths of each of the four linkage components (Figure 1) were controlled by 4 independent loci (2 alleles at each locus). Links themselves were modeled to be genetically independent of one another. The effect of each allele was assumed to be equal and additive. Importantly, the assumptions of (i) number of loci per link, (ii) genetic independence of links and (iii) additivity of allelic affects are supported by empirical quantitative genetic data for the cichlid craniofacial skeleton . For example, even though the lower jaw and maxilla links are positively (phenotypically) correlated in our data set, this is unlikely to be due to genetic linkage; QTL for the shape of these elements map to distinct chromosomal regions. We used this model to (a) determine if MTOM species would produce hybrids transgressive for function, (b) estimate the percentage of F2 progeny exhibiting transgression from specific Lake Malawi cichlid intercrosses, and (c) investigate the genetic contribution of each link to the phenomenon of functional transgression.
Simulated crosses of Lake Malawi cichlids produce transgression at appreciable frequencies.
Cynotilapia afra × Pseudotropheus elongatus
Protomelas fenestratus × Protomelas ornatus
Chilotilapia rhoadesii × Maravichromis subocularis
Copadichromis quadrimaculatus × Corematodus taeniatus
Cynotilapia afra × Metriaclima zebra
Protomelas ornatus × Protomelas taeniolatus
Protomelas spilopterus 'blue' × Protomelas fenestratus
Copadichromis virginalis × Chilotilapia rhoadesii
Petrotilapia nigra × Pseudotropheus elongatus
Metriaclima zebra × Labeotropheus trewavasae
Nimbochromis polystigma × Chilotilapia rhoadesii
Pseudotropheus elongatus × Labeotropheus fuelleborni
Metriaclima zebra × Pseudotropheus elongatus
Copadichromis mloto × Otopharynx picta
Labidochromis vellicans × Pseudotropheus elongatus
Ps. Tropheops 'orange chest' × Ps. Tropheus 'red cheek'
Copadichromis quadrimaculatus × Dimidochromis compressiceps
Copadichromis virginalis × Lethrinops altus
Copadichromis virginalis × Tyrannochromis macrostoma
Ps. Tropheops 'orange chest' × Labeotropheus fuelleborni
We have described a general and likely pervasive mechanism that generates functional novelty. Simulated hybrid offspring among Lake Malawi cichlids exhibiting MTOM are transgressive for function at appreciable frequency. Our modeling approach is noteworthy because it allows us to identify morphological components of the 4-bar mechanical system that contribute to TS. Functional transgression is a product of recombination and assortment between alleles controlling the lengths of the lower jaw and the maxilla and occurs in the absence of transgressive morphology. Transgression occurs when link lengths approaching parental values assort in new combinations in the F2 generation. Novel function therefore is realized via new morphological combinations, but not transgressive lengths for any single link. Our model can be tested by breeding Malawi cichlid hybrids in the lab and examining the morphological and mechanical diversity of their 4-bar linkages.
It is important to comment that the model we present shows how MTOM of form to function in the Malawi cichlid 4-bar linkage could generate TS in jaw biomechanics. One question raised by the modeling results is why mbuna species have not evolved higher maxillary KT (mbuna range = 0.58 – 0.85). What maintains the positive phenotypic correlation between the lower jaw and maxilla links? One possibility is functional constraint imposed by other aspects of the feeding apparatus. For example, the lower jaw and maxilla both function to position the oral jaws for occlusion and contribute to the gape of the mouth. Mismatches in the length of upper and lower jaw elements may have negative functional ramifications that outweigh increased performance in jaw speed.
Recombinational evolution, MTOM and the limits to functional diversity
The genomic era has changed the way that evolutionary biologists think about hybridization. Gene flow among recently diverged species (or those evolved through pre-mating barriers) is common rather than the exception [13, 15, 29]. Hybridization may provide an important source of genetic variation in the form of new trait combinations  that sometimes help hybrid organisms maneuver across fitness landscapes . The phenomenon of TS, wherein hybrids outperform the parents, is a frequent observation in laboratory and natural outcrossings .
It has been suggested that strong directional selection and simple genetic architecture should limit TS because they point the phenotypic effects of QTL in the same direction; this would essentially constrain diversification by hybridization . Our analysis shows how MTOM promotes TS in function, without transgressive morphology, via recombination and independent assortment. Because multiple morphological solutions exist for any function (i.e., value of KT), MTOM may buffer those constraints, imposed by directional selection, on the extent of mechanical diversity produced by hybridization. As the craniofacial skeleton evolves, functional demands of numerous mechanical systems shape the lengths and linkages of bony elements . MTOM of form to function in each of these systems might facilitate, or perhaps even require, the evolution of diversity.
Cichlid specimens were collected during July 2005 from various sites in southern Lake Malawi. Fishes were labeled with a unique identifier and fixed in 10% buffered formalin solution. Upon returning to the U.S., carcasses were transferred to 70% ethanol for storage. Additional specimens were borrowed from the American Museum of Natural History (AMNH) to supplement the collection. Up to three individuals of each species (depending on the number available) were cleared with trypsin and double-stained using alcian-blue (cartilage) and alizarin-red (bone). This method allows clear visualization of the skeletal components while maintaining skull articulations . Cleared and stained fish were transferred to glycerin for storage.
Morphometrics and correlation
We measured the anterior jaw 4-bar linkage model as described [26, 38, 39]. The four physical units of the linkage were quantified on 169 specimens of 86 Lake Malawi cichlid species. Up to three individuals were measured for each species using dial calipers (nearest 0.1 mm) to quantify each link (Figure 1). The four links (lower jaw or input, maxilla or output, nasal or coupler, and fixed or suspensorium) are described in detail, with their respective measurement landmarks, by Hulsey and Wainwright . The linkage measurements were used to calculate the kinematic transmission (KT) of each jaw . Anterior jaw KT is used as an estimate of the speed of motion transmitted through the 4-bar linkage, and in addition, the measurement of KT simultaneously describes the force transmission (FT) through the 4-bar as the reciprocal of KT . The method of KT calculation followed that of Hulsey and Garcia de León  and was accomplished using an iterative function in Microsoft Excel® with a starting angle of 15° and an input angle of 30°.
Correlations were calculated between each of the 4-bar links and KT to examine the relationship therein. Because the structural components of the anterior jaw are highly correlated with body size [, NFP unpublished] each 4-bar link was corrected for fish standard length (SL) prior to correlation. We used the residuals of linear regression of link length to SL. Felsenstein  has shown that correlations may not be statistically independent when compared across taxa with common evolutionary history. Therefore, we calculated phylogenetically independent contrasts following an approach outlined in Hulsey et al. . We constructed a phylogeny of 52 Lake Malawi species using sequences from the mitochondrial ND2 gene [see Additional file 1, Additional file 3]. All species were collected from the wild in Lake Malawi from various locations. DNA extractions, PCR parameters, and sequencing followed previously published protocols .
The ND2 gene was transformed into its three codon partitions. ModelTest 3.06  was used to identify the most likely model of molecular evolution for each codon partition. Standard Bayesian analyses were executed to find the maximum log-likelihood topology using MrBayes 3.0 . Independent contrast analyses were performed using CAIC  in order to assess correlations among the SL-corrected residuals of the four link lengths and among those values and KT. We employed the highest log-likelihood tree from the above Bayesian search to correct for phylogeny [Additional file 3].
Genetic model of hybrid crosses
Several approaches can be taken to model the generation of novelty in jaw structures and for this project we chose a simple genetic model. Previous studies have examined how 4-bar function changes with different structural configurations, as well as how the 4-bar can evolve based on selection for different KT [25, 26, 43, 44]. Also, Albertson and Kocher  have examined the phenotypic distribution of one interspecific Lake Malawi cross in terms of cranial and jaw morphology. For this paper we wanted a model that would not only describe the distribution of genotypes and phenotypes for specific intercrosses, but also allow the incorporation of empirical data from the Lake Malawi system.
We constructed a simple but realistic individual-based Mendelian genetic model, which incorporated assumptions of no mutation, no selection, and no error. We assumed that the size-standardized (below) length of each of the four anterior jaw links was controlled by 4 independent loci with 2 alleles at each locus, for a total of 8 alleles per link. Links themselves were modeled to be genetically independent of one another. The effect of each allele was assumed to be equal and additive, and therefore each of the four lengths (lower jaw, maxilla, nasal, fixed) for each parental (or F0) specimen was divided by 8. Note that the assumptions of (i) number of loci per link, (ii) independence of links and (iii) additivity of allelic affects are supported by empirical quantitative genetic data for the cichlid craniofacial skeleton . We controlled for differences in body size among species in the model by dividing each parental link length by SL. In this way, the heritable unit of link length can be thought of as the proportion of SL made up by each link. We also ran models using residuals from linear regression of link length on SL as input variables, and this did not change the outcome.
Using this rubric, each allele inherited from a parent would impart 1/8th of the total length of that link to the offspring. Parents were assumed to be homozygous at all loci. The initial cross among F0 produced F1 progeny with identical 4-bar lengths (and KT values) equal to the average of the two parents. A second cross within the F1 progeny produced all potential parental and recombinant genotypes in the F2 generation (6,561 possible). Hybrid link lengths were calculated by the summation of all allelic contributions totaled over the four loci per link. Thus, each composite F2 genotype was assigned a 4-link phenotype, and KT was calculated for all. Some recombinant link lengths did not support a functional jaw linkage in some crosses. This result was taken to represent potentially unfit hybrid individuals within a cross and these individuals were left out of further analyses; this effect has been noted in prior simulation . Frequency distributions of F2 progeny were created (MS Excel® and SigmaPlot® 8.0) to compare hybrid KT values to parental KT. Bubble plots were generated (SigmaPlot® 8.0) to examine the contribution of parental alleles to link length in F2 exhibiting transgressive KT. A total of 20 interspecific crosses were simulated with this model and F2 KT values were examined for evidence of transgression. Species were chosen for these 20 iterations (i) if there is a report of hybridization between them in nature, (ii) if laboratory hybrids have been made, or (iii) if we were particularly interested in the cross from inspection of parental morphometrics.
These 20 simulated crosses present a biased look at the possibility of transgressive function in Lake Malawi cichlid hybrids. The calculations are iterative and time consuming. We wanted an unbiased means to ask if a hybrid cross between any two species would produce F2 with transgressive KT. To accomplish this, we made use of the tight relationship between the fully parameterized model of KT and the simpler ratio of input to output links (Figure 3) and the relationship between input link, output link and KT observed in our data (see Results) and from previous simulation [25, 26]. We generated a 86 × 86 species matrix containing all possible combinations of size-adjusted lower jaw and maxilla lengths from all species in the data set (7,310 combinations). We essentially asked if recombining the maxilla from one species with the lower jaw from the other (and vice versa) would produce hybrid linkages transgressive in KT. We carried out this operation for all pairs of species in the data set.
We thank members of the Streelman lab for comments on previous drafts of the manuscript. The research is supported by grants from the NSF (IOB 0546423) and the Alfred P. Sloan Foundation (BR 4499) to JTS.
- Gerhart J, Kirschner M: Cells, embryos, and evolution: Toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability. 1997, Malden: Blackwell ScienceGoogle Scholar
- Raymond J, Segre D: The effect of oxygen on biochemical networks and the evolution of complex life. Science. 2006, 311: 1764-1767. 10.1126/science.1118439.View ArticlePubMedGoogle Scholar
- Lawton-Rauh AL, Alvarez-Buylla ER, Purugganan MD: Molecular evolution of flower development. Trends Ecol Evol. 2000, 15: 144-149. 10.1016/S0169-5347(99)01816-9.View ArticlePubMedGoogle Scholar
- Shubin N, Tabin C, Carroll S: Fossils, genes and the evolution of animal limbs. Nature. 1997, 388: 639-648. 10.1038/41710.View ArticlePubMedGoogle Scholar
- Gans C, Northcutt RG: Neural crest and the origin of vertebrates: a new head. Science. 1983, 220: 268-274. 10.1126/science.220.4594.268.View ArticlePubMedGoogle Scholar
- Streelman JT, Peichel CL, Parichy DM: Developmental genetics of adaptation in fishes: the case for novelty. Ann Rev Ecol Evol Syst. 2007, 38: 655-681. 10.1146/annurev.ecolsys.38.091206.095537.View ArticleGoogle Scholar
- Grant PR, Grant BR: Hybridization of bird species. Science. 1992, 256: 193-197. 10.1126/science.256.5054.193.View ArticlePubMedGoogle Scholar
- Barton NH: The role of hybridization in evolution. Mol Ecol. 2001, 10: 551-568. 10.1046/j.1365-294x.2001.01216.x.View ArticlePubMedGoogle Scholar
- Burke JM, Arnold ML: Genetics and the fitness of hybrids. Ann Rev Gen. 2001, 35: 31-52. 10.1146/annurev.genet.35.102401.085719.View ArticleGoogle Scholar
- Rieseberg LH, Raymond O, Rosenthal KM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzback AE, Donovan LA, Lexer C: Major ecological transitions in wild sunflowers facilitated by hybridization. Science. 2003, 301: 1211-1216. 10.1126/science.1086949.View ArticlePubMedGoogle Scholar
- Grant PR, Grant BR: High survival of Darwin's finch hybrids: effects of beak morphology and diets. Ecology. 1996, 77: 500-509. 10.2307/2265625.View ArticleGoogle Scholar
- Ellstrand NC, Schierenbeck KA: Hybridization as a stimulus for the evolution of invasiveness in plants?. Proc Natl Acad Sci. 2000, 97: 7043-7050. 10.1073/pnas.97.13.7043.PubMed CentralView ArticlePubMedGoogle Scholar
- Seehausen O: Hybridization and adaptive radiation. Trends Ecol Evol. 2004, 19: 198-207. 10.1016/j.tree.2004.01.003.View ArticlePubMedGoogle Scholar
- Mallet J: Hybrid speciation. Nature. 2007, 446: 279-283. 10.1038/nature05706.View ArticlePubMedGoogle Scholar
- Grant P, Grant BR, Markert JA, Keller LF, Petren K: Convergent evolution of Darwin's finches caused by introgressive hybridization and selection. Evolution. 2004, 58: 1588-1599.View ArticlePubMedGoogle Scholar
- Rieseberg LH, Whitton J, Gardner K: Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics. 1999, 152: 713-727.PubMed CentralPubMedGoogle Scholar
- Lexer C, Welch ME, Raymond O, Rieseberg LH: The origin of ecological divergence in Helianthus paradoxus (Asteraceae): selection on transgressive characters in a novel hybrid habitat. Evolution. 2003, 57: 1989-2000.View ArticlePubMedGoogle Scholar
- Rieseberg LH, Archer MA, Wayne RK: Transgressive segregation, adaptation and speciation. Heredity. 1999, 83: 363-372. 10.1038/sj.hdy.6886170.View ArticlePubMedGoogle Scholar
- Rieseberg LH, Widmer A, Arntz AM, Burke JM: Directional selection is the primary cause of phenotypic diversification. Proc Natl Acad Sci. 2002, 99: 12242-12245. 10.1073/pnas.192360899.PubMed CentralView ArticlePubMedGoogle Scholar
- Orr HA: Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics. 1998, 149: 2099-2104.PubMed CentralPubMedGoogle Scholar
- Albertson RC, Kocher TD: Genetic architecture sets limits on transgressive segregation in hybrid cichlid fishes. Evolution. 2005, 59: 686-690.View ArticlePubMedGoogle Scholar
- Albertson RC, Streelman JT, Kocher TD: Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proc Natl Acad Sci. 2003, 100: 5252-5257. 10.1073/pnas.0930235100.PubMed CentralView ArticlePubMedGoogle Scholar
- Albertson RC, Streelman JT, Kocher TD, Yelick PC: Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proc Natl Acad Sci. 2005, 102: 16287-16292. 10.1073/pnas.0506649102.PubMed CentralView ArticlePubMedGoogle Scholar
- Streelman JT, Albertson RC: Evolution of novelty in cichlid dentition. J Exper Zool MDE. 2006, 306b: 216-226. 10.1002/jez.b.21101.View ArticleGoogle Scholar
- Alfaro ME, Bolnick DI, Wainwright PC: Evolutionary dynamics of complex biomechanical systems: an example using the four-bar mechanism. Evolution. 2004, 58: 495-503.View ArticlePubMedGoogle Scholar
- Hulsey CD, Wainwright PC: Projecting mechanics into morphospace: disparity in the feeding system of labrid fishes. Proc Biol Sci. 2002, 269: 317-326. 10.1098/rspb.2001.1874.PubMed CentralView ArticlePubMedGoogle Scholar
- Hulsey CD, Garcia de Leon FJ: Cichlid jaw mechanics: linking morphology to feeding specialization. Funct Ecol. 2005, 19: 487-494. 10.1111/j.1365-2435.2005.00987.x.View ArticleGoogle Scholar
- Hulsey CD, Fraser GJ, Streelman JT: Evolution and development of complex biomechanical systems: 300 million years of fish jaws. Zebrafish. 2005, 2: 243-257. 10.1089/zeb.2005.2.243.View ArticlePubMedGoogle Scholar
- Won Y-J, Sivasundar A, Wang Y, Hey J: On the origin of Lake Malawi cichlid species. Proc Natl Acad Sci USA. 2005, 102: 6581-6586. 10.1073/pnas.0502127102.PubMed CentralView ArticlePubMedGoogle Scholar
- Hulsey CD, Mims MC, Streelman JT: Do constructional constraints influence cichlid craniofacial diversification?. Proc Roy Soc Lond B. 2007, 274: 1867-1875. 10.1098/rspb.2007.0444.View ArticleGoogle Scholar
- Smith PF, Kornfield I: Phylogeography of Lake Malawi cichlids of the genus Pseudotropheus : significance of allopatric colour variation. Proc Roy Soc Lond B. 2002, 269: 2495-2502. 10.1098/rspb.2002.2188.View ArticleGoogle Scholar
- Smith PF, Konings A, Kornfield I: Hybrid origin of a cichlid population in Lake Malawi: implications for genetic variation and species diversity. Mol Ecol. 2003, 12: 2497-2504. 10.1046/j.1365-294X.2003.01905.x.View ArticlePubMedGoogle Scholar
- Streelman JT, Gmyrek SL, Kidd MR, Kidd C, Robinson RL, Hert E, Ambali AJ, Kocher TD: Hybridization and contemporary evolution in an introduced cichlid fish from Lake Malawi National Park. Mol Ecol. 2004, 13: 2471-2479. 10.1111/j.1365-294X.2004.02240.x.View ArticlePubMedGoogle Scholar
- Wainwright PC, Bellwood DR, Westneat MW, Grubich JR, Hoey AS: A functional morphospace for the skull of labrid fishes: patterns of diversity in a complex biomechanical system. Biol J Linn Soc. 2004, 82: 1-25. 10.1111/j.1095-8312.2004.00313.x.View ArticleGoogle Scholar
- Westneat MW, Alfaro ME, Wainwright PC, Bellwood DR, Grubich JR, Fessler JL, Clements KD, Smith LL: Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae. Proc Roy Soc Lond B. 2005, 272: 993-1000. 10.1098/rspb.2004.3013.View ArticleGoogle Scholar
- Felsenstein J: Phylogenies from gene-frequencies – a statistical problem. Syst zool. 1985, 34: 300-311. 10.2307/2413149.View ArticleGoogle Scholar
- Won Y-J, Wang Y, Sivasundar A, Raincrow J, Hey J: Nuclear gene variation and molecular dating of the cichlid species flock of Lake Malawi. Mol biol evol. 2006, 23: 828-837. 10.1093/molbev/msj101.View ArticlePubMedGoogle Scholar
- Westneat MW: Feeding mechanics of teleost fishes (Labridae, Perciformes) – a test of 4-bar linkages. Journal of morphology. 1990, 205: 269-295. 10.1002/jmor.1052050304.View ArticleGoogle Scholar
- Muller M: A novel classification of planar four-bar linkages and its application to the mechanical analysis of animal systems. Philos Trans Roy Soc Lond B. 1996, 351: 689-720. 10.1098/rstb.1996.0065.View ArticleGoogle Scholar
- Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998, 14: 817-818. 10.1093/bioinformatics/14.9.817.View ArticlePubMedGoogle Scholar
- Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.View ArticlePubMedGoogle Scholar
- Purvis A, Rambaut A: Comparative-analysis by independent contrasts (CAIC) – an Apple-Macintosh application for analyzing comparative data. Computer applications in the biosciences. 1995, 11: 247-251.PubMedGoogle Scholar
- Alfaro ME, Bolnick DI, Wainwright PC: Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in Labrid fishes. The American naturalist. 2005, 165: 141-154. 10.1086/429564.View ArticleGoogle Scholar
- Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD: Many-to-one mapping of form to function: a general principle in organismal design?. Integrative and comparative biology. 2005, 45: 256-262. 10.1093/icb/45.2.256.View ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.