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The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis Chilotes X H

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The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis Chilotes X H INVESTIGATION The Integrated Genomic Architecture and Evolution of Dental Divergence in East African Cichlid Fishes (Haplochromis chilotes x H. nyererei) C. Darrin Hulsey,*,1 Gonzalo Machado-Schiaffino,* Lara Keicher,* Diego Ellis-Soto,* Frederico Henning,*,† and Axel Meyer* *Department of Biology, University of Konstanz, 78457, Germany and †Department of Genetics, Federal University of Rio de Janeiro, 21941, Brazil ORCID ID: 0000-0002-9653-6728 (C.D.H.) ABSTRACT The independent evolution of the two toothed jaws of cichlid fishes is thought to have KEYWORDS promoted their unparalleled ecological divergence and species richness. However, dental divergence in adaptive cichlids could exhibit substantial genetic covariance and this could dictate how traits like tooth numbers radiation evolve in different African Lakes and on their two jaws. To test this hypothesis, we used a hybrid mapping key innovation cross of two trophically divergent Lake Victoria species (Haplochromis chilotes · Haplochromis nyererei)to natural selection examine genomic regions associated with cichlid tooth diversity. Surprisingly, a similar genomic region was QTL found to be associated with oral jaw tooth numbers in cichlids from both Lake Malawi and Lake Victoria. trophic evolution Likewise, this same genomic location was associated with variation in pharyngeal jaw tooth numbers. Similar relationships between tooth numbers on the two jaws in both our Victoria hybrid population and across the phylogenetic diversity of Malawi cichlids additionally suggests that tooth numbers on the two jaws of haplochromine cichlids might generally coevolve owing to shared genetic underpinnings. Integrated, rather than independent, genomic architectures could be key to the incomparable evolutionary divergence and convergence in cichlid tooth numbers. The subdivision of organisms into distinct developmental genetic limbs, or vertebrate teeth are able to evolve independently and sub- modules or units greatly influences the evolution of biological diversity. sequently become specialized with respect to other homologous organs, Similar to processes such as speciation (Slowinski and Guyer 1993; this can heavily influence a clade’s evolutionary success (Wagner and Elmer et al. 2014) and gene duplication (Meyer and Schartl 1999; Altenberg 1996; Stock 2001; Edwards and Weinig 2011; Santana and Taylor et al. 2001; Wagner 2008; Ohno 2013) that both increase the Lofgren 2013; Miller et al. 2014). For instance, the capacity of the two particulate nature of biological entities, segmentation of organisms into jaws of cichlid fishes to evolve independently has been commonly in- serially homologous units has been suggested to be a major facilitator of voked as a critical catalyst underlying both the unparalleled trophic diversification (Wagner 1996). When particular plant leaves, arthropod divergence of these fishes and the phenomenal convergence that char- acterizes their adaptive radiations (Liem 1973; Hulsey et al. 2006). Copyright © 2017 Hulsey et al. However, the degree to which particular parts of phenotypes can evolve doi: https://doi.org/10.1534/g3.117.300083 independently and contribute to adaptation might be largely a result of Manuscript received June 30, 2017; accepted for publication July 25, 2017; their underlying genetic architectures (Lande 1984; Albertson and published Early Online July 27, 2017. Kocher 2006; Brakefield 2006; Wilkens 2010; Albertson et al. 2014; This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/ Armbruster et al. 2014; Gross et al. 2016). Structures ranging from licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction flower pistils to snake vertebrae to primate teeth have been suggested in any medium, provided the original work is properly cited. to evolve largely according to their genetic covariance (Schluter 1996; Supplemental material is available online at www.g3journal.org/lookup/suppl/ Hohenlohe and Arnold 2008; Hlusko 2016; Smith 2016). Likewise, doi:10.1534/g3.115.023366/-/DC1. 1Corresponding author: Chair in Zoology and Evolutionary Biology, Department of genomic architecture may have constrained even the astounding phe- Biology, University of Konstanz, Bldg. M, Room M808, Universitatsstrasse 10, notypic diversity of cichlid teeth. To better understand the factors Konstanz 78457, Germany. E-mail: [email protected] structuring trophic evolution in one of the most species-rich vertebrate Volume 7 | September 2017 | 3195 radiations on Earth, we examined the genomic substrate of tooth number therefore, parallelism could be rare in the extraordinarily species-rich divergence on both the oral and pharyngeal jaws of East African cichlids. East African Rift Lakes. Although Lake Malawi and Lake Victoria each Most groups of fish have two toothed jaws (Schaeffer and Rosen contain several hundred species, all of these species have diverged 1961; Figure 1). They have oral jaws that are largely homologous to our extremely rapidly (2 MYA) from a common ancestor (Genner et al. jaws and are used primarily to capture prey, and they also have pha- 2007; Friedman et al. 2013). Interspecificgeneflowamongmanyofthese ryngeal jaws, which are modified gill arches, that are used to macerate recently diverged lineages also still occurs occasionally (Mims et al. 2010; and process prey (Liem 1973). However, unlike any other group of fish, Holzman and Hulsey 2017). These aspects of their evolutionary past cichlids exhibit an incredible amount of diversity in the shape, size, and have likely contributed to the considerable sharing of ancestral molecular number of teeth on both of their jaws (Fryer and Iles 1972). Because polymorphisms observed even among cichlid lineages that are geograph- several lines of evidence have supported the functional as well as the ically separated (Loh et al. 2008; Brawand et al. 2014). However, whether evolutionary independence of the two jaws (Liem 1973; Hulsey et al. or not these shared ancestral polymorphisms contribute to phenotypic 2006), cichlid oral and pharyngeal teeth might commonly change in- divergence or even repeatedly evolved parallel adaptations is not known. dependently to promote the distinct trophic roles of their two jaws. But because our understanding of genomic architecture is rapidly in- Divergence in teeth could most often be the result of genes that are creasing in African cichlid radiations (Brawand et al. 2014; Henning and specifically involved in forming teeth on only one jaw. Yet at least 30% Meyer 2014), we can now begin to compare whether similar genomic of the genes found to be involved in forming mouse teeth are also regions do underlie divergence in similar phenotypes between evolution- expressed in both tooth-bearing jaws of cichlids (Hulsey et al. 2016). arily distinct clades of cichlids. For instance, several quantitative trait loci This suggests that there is likely a substantial degree of developmental (QTL) for oral jaw tooth number were recently identified in a hybrid similarity, or integration at the level of gene expression, in teeth on cross of Lake Malawi cichlids (Bloomquist et al. 2015), and these same these morphologically and evolutionarily distinct jaws. Also, despite the loci might be playing a part in tooth divergence in many closely related distinct evolutionary origin of the two sets of jaws, the evolution of cichlids. To test this idea, additional hybrid crosses of species with dif- tooth number on both the oral and pharyngeal jaws across a diversity of ferent dentitions could be used to determine whether the same genomic Malawi cichlids is highly and positively correlated (Fraser et al. 2009). regions responsible for phenotypic divergence in tooth number are Therefore, the genomic architecture dictating dental divergence on shared across distinct cichlid clades. both cichlid jaws could be highly similar. The genetic underpinnings of traits are often thought to influence or Cichlid fishes are well known for the repeated independent evolution even constrain how they diversify (Lande 1984; Schluter 1996). How- of similar features in different lineages (Fryer and Iles 1972; Rüber et al. ever, there are very few examples where the genetic correlations among 1999; Brawand et al. 2014). Their rampant convergence is also often traits are known in similar taxa in which we understand the degree to used as an iconic example of how natural selection can deterministically which traits coevolve over phylogenetic scales (Brakefield 2006). Yet we shape diversity (Henning and Meyer 2014; Machado-Schiaffino et al. are increasingly dissecting the genomic basis of traits such as flower 2015). For instance, in environments such as Lakes Victoria and pistil and stamen lengths, mammalian limb lengths, and the size of Malawi, phylogenetically distinct lineages of cichlids have colonized different hominid teeth, which have also been examined in a phyloge- each lake independently from riverine environments and then, within netically informed context (Hlusko 2016; Smith 2016). Combining very short timeframes, repeatedly evolved similar feeding specializa- genetic crosses with comparative analyses, should allow us to determine tions (Meyer et al. 1990; Meyer 1993; Genner et al. 2007; Hulsey et al. whether levels of genomic integration can predict the degree to which 2010). These convergent trophic phenotypes such as algae scraping, traits change in concert across their macro-evolutionary history. For
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