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1.  Evolution of genomic structural variation and genomic architecture in the adaptive radiations of African cichlid fishes 
Frontiers in Genetics  2014;5:163.
African cichlid fishes are an ideal system for studying explosive rates of speciation and the origin of diversity in adaptive radiation. Within the last few million years, more than 2000 species have evolved in the Great Lakes of East Africa, the largest adaptive radiation in vertebrates. These young species show spectacular diversity in their coloration, morphology and behavior. However, little is known about the genomic basis of this astonishing diversity. Recently, five African cichlid genomes were sequenced, including that of the Nile Tilapia (Oreochromis niloticus), a basal and only relatively moderately diversified lineage, and the genomes of four representative endemic species of the adaptive radiations, Neolamprologus brichardi, Astatotilapia burtoni, Metriaclima zebra, and Pundamila nyererei. Using the Tilapia genome as a reference genome, we generated a high-resolution genomic variation map, consisting of single nucleotide polymorphisms (SNPs), short insertions and deletions (indels), inversions and deletions. In total, around 18.8, 17.7, 17.0, and 17.0 million SNPs, 2.3, 2.2, 1.4, and 1.9 million indels, 262, 306, 162, and 154 inversions, and 3509, 2705, 2710, and 2634 deletions were inferred to have evolved in N. brichardi, A. burtoni, P. nyererei, and M. zebra, respectively. Many of these variations affected the annotated gene regions in the genome. Different patterns of genetic variation were detected during the adaptive radiation of African cichlid fishes. For SNPs, the highest rate of evolution was detected in the common ancestor of N. brichardi, A. burtoni, P. nyererei, and M. zebra. However, for the evolution of inversions and deletions, we found that the rates at the terminal taxa are substantially higher than the rates at the ancestral lineages. The high-resolution map provides an ideal opportunity to understand the genomic bases of the adaptive radiation of African cichlid fishes.
PMCID: PMC4042683  PMID: 24917883
SNPs; insertions; deletions; inversions; adaptive radiation; structural variation
2.  The Gut Microbial Community of Midas Cichlid Fish in Repeatedly Evolved Limnetic-Benthic Species Pairs 
PLoS ONE  2014;9(4):e95027.
Gut bacterial communities are now known to influence a range of fitness related aspects of organisms. But how different the microbial community is in closely related species, and if these differences can be interpreted as adaptive is still unclear. In this study we compared microbial communities in two sets of closely related sympatric crater lake cichlid fish species pairs that show similar adaptations along the limnetic-benthic axis. The gut microbial community composition differs in the species pair inhabiting the older of two crater lakes. One major difference, relative to other fish, is that in these cichlids that live in hypersaline crater lakes, the microbial community is largely made up of Oceanospirillales (52.28%) which are halotolerant or halophilic bacteria. This analysis opens up further avenues to identify candidate symbiotic or co-evolved bacteria playing a role in adaptation to similar diets and life-styles or even have a role in speciation. Future functional and phylosymbiotic analyses might help to address these issues.
PMCID: PMC3986361  PMID: 24733403
3.  Crater lake cichlids individually specialize along the benthic–limnetic axis 
Ecology and Evolution  2014;4(7):1127-1139.
A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of elongated open water (limnetic) species and high-bodied shore (benthic) species from generalist ancestors. Studies on phenotype-diet correlations have suggested that population-wide individual specialization occurs at an early evolutionary and ecological stage of divergence and niche partitioning. This variable restricted niche use across individuals can provide the raw material for earliest stages of sympatric divergence. We investigated variation in morphology and diet as well as their correlations along the benthic-limnetic axis in an extremely young Midas cichlid species, Amphilophus tolteca, endemic to the Nicaraguan crater lake Asososca Managua. We found that A. tolteca varied continuously in ecologically relevant traits such as body shape and lower pharyngeal jaw morphology. The correlation of these phenotypes with niche suggested that individuals are specialized along the benthic-limnetic axis. No genetic differentiation within the crater lake was detected based on genotypes from 13 microsatellite loci. Overall, we found that individual specialization in this young crater lake species encompasses the limnetic-as well as the benthic macro-habitat. Yet there is no evidence for any diversification within the species, making this a candidate system for studying what might be the early stages preceding sympatric divergence.
A common pattern of adaptive diversification in freshwater fishes is the repeated evolution of open water (limnetic) species and of shore (benthic) species. Individual specialization can reflect earliest stages of evolutionary and ecological divergence. We here demonstrate individual specialization along the benthic–limnetic axis in a young adaptive radiation of crater lake cichlid fishes.
PMCID: PMC3997327  PMID: 24772288
Benthic–limnetic axis; divergent selection; ecological opportunity; individual specialization; parallel evolution; phenotype-diet correlation
4.  Introgressive hybridization and latitudinal admixture clines in North Atlantic eels 
Hybridization, the interbreeding of diagnosably divergent species, is a major focus in evolutionary studies. Eels, both from North America and Europe migrate through the Atlantic to mate in a vast, overlapping area in the Sargasso Sea. Due to the lack of direct observation, it is unknown how these species remain reproductively isolated. The detection of inter-species hybrids in Iceland suggests on-going gene flow, but few studies to date have addressed the influence of introgression on genetic differentiation in North Atlantic eels.
Here, we show that while mitochondrial lineages remain completely distinct on both sides of the Atlantic, limited hybridization is detectable with nuclear DNA markers. The nuclear hybridization signal peaks in the northern areas and decreases towards the southern range limits on both continents according to Bayesian assignment analyses. By simulating increasing proportions of both F1 hybrids and admixed individuals from the southern to the northern-most locations, we were able to generate highly significant isolation-by-distance patterns in both cases, reminiscent of previously published data for the European eel. Finally, fitting an isolation-with-migration model to our data supports the hypothesis of recent asymmetric introgression and refutes the alternative hypothesis of ancient polymorphism.
Fluctuating degrees of introgressive hybridization between Atlantic eel species are sufficient to explain temporally varying correlations of geographic and genetic distances reported for populations of the European eel.
PMCID: PMC3986858  PMID: 24674242
Anguilla anguilla; Anguilla rostrata; Gene flow; Isolation-by-distance; Simulation; Migration barriers
5.  Revisiting de Beer’s textbook example of heterochrony and jaw elongation in fish: calmodulin expression reflects heterochronic growth, and underlies morphological innovation in the jaws of belonoid fishes 
EvoDevo  2014;5:8.
Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches. Understanding the nature of these developmental events can provide insights into fundamental molecular mechanisms of evolutionary change. Fishes from the Suborder Belonoidei display a vast array of extreme craniofacial morphologies that appear to have arisen through a series of heterochronic shifts. We performed a molecular heterochrony study, comparing postembryonic jaw development in representatives of the Suborder Belonoidei, the halfbeak Dermogenys pusilla (where the lower jaw is considerably elongated compared to the upper jaw) and the needlefish Belone belone (where both jaws are elongated), to a representative of their sister group the Suborder Adrianichthyoidei, the medaka Oryzias latipes, which has retained the ancestral morphology.
Early in development, the lower jaw displays accelerated growth both in needlefish and halfbeak compared to medaka, and secondary acceleration of the upper jaw is seen in needlefish later in their development, representing a case of mosaic heterochrony. We identified toothless extensions of the dentaries as innovations of Belonoid fishes and the source of heterochronic growth. The molecular basis of growth heterochronies in the Belonoidei was examined through comparing expression of skeletogenic genes during development of halfbeak and medaka. The calmodulin paralogue calm1 was identified as a potential regulator of jaw length in halfbeak as its expression gradually increases in the lower jaw, but not the upper jaw, in a pattern that matches its outgrowth. Moreover, medaka displays equal expression of calm1 in the upper and lower jaws, consistent with the lack of jaw outgrowth in this species.
Heterochronic shifts in jaw growth have occurred repeatedly during the evolution of Belonoid fishes and we identify toothless extensions of the dentaries as an important innovation of this group. Our results suggest that calm1 contributes to jaw heterochrony in halfbeak, potentially driving further heterochronic shifts in jaw growth across the Suborder Belonoidei, such as the upper jaw acceleration observed in needlefish.
PMCID: PMC3927394  PMID: 24499543
Heterochrony; Morphological innovation; Jaw development; Beloniformes; Gavin de Beer; Dermogenys; Belone; Medaka; Calmodulin
6.  The Imprinted NPAP1 Gene in the Prader–Willi Syndrome Region Belongs to a POM121-Related Family of Retrogenes 
Genome Biology and Evolution  2014;6(2):344-351.
We have recently shown that the human Nuclear pore-associated protein (NPAP1)/C15orf2 gene encodes a nuclear pore-associated protein. This gene is one of several paternally expressed imprinted genes in the genomic region 15q11q13. Because the Prader–Willi syndrome is known to be caused by the loss of function of paternally expressed genes in 15q11q13, a phenotypic contribution of NPAP1 cannot be excluded. NPAP1 appears to be under strong positive Darwinian selection in primates, suggesting an important function in primate biology. Interestingly, however, in contrast to all other protein-coding genes in 15q11q13, NPAP1 has no ortholog in the mouse. Our investigation of the evolutionary origin of NPAP1 showed that the gene is specific to primate species and absent from the 15q11q13-orthologous regions in all nonprimate mammals. However, we identified a group of paralogous genes, which we call NPAP1L, in all placental mammals except rodents. Phylogenetic analysis revealed that NPAP1, NPAP1L, and another group of genes (UPF0607), which is also restricted to primates, are closely related to the vertebrate transmembrane nucleoporin gene POM121, although they lack the transmembrane domain. These three newly identified groups of genes all lack conserved introns, and hence, are likely retrogenes. We hypothesize that, in the common ancestor of placentals, the POM121 gene retrotransposed and gave rise to an NPAP1-ancestral retrogene NPAP1L/NPAP1/UPF0607. Our results suggest that the nuclear pore-associated gene NPAP1 originates from the vertebrate nucleoporin gene POM121 and—after several steps of retrotransposition and duplication—has been subjected to genomic imprinting and positive selection after integration into the imprinted SNRPN-UBE3A chromosomal domain.
PMCID: PMC3942032  PMID: 24482533
C15orf2; NPAP1L; UPF0607; imprinting; nucleoporin; nuclear pore complex
7.  Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all 
Individuals of the scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika tend to have remarkably asymmetric heads that are either left-bending or right-bending. The ‘left’ morph opens its mouth markedly towards the left and preferentially feeds on the scales from the right-hand side of its victim fish, and the ‘right’ morph bites scales from the victims’ left-hand side. This striking dimorphism made these fish a textbook example of their astonishing degree of ecological specialization and as one of the few known incidences of negative frequency-dependent selection acting on an asymmetric morphological trait, where left and right forms are equally frequent within a species. We investigated the degree and the shape of the frequency distribution of head asymmetry in P. microlepis to test whether the variation conforms to a discrete dimorphism, as generally assumed. In both adult and juvenile fish, mouth asymmetry appeared to be continuously and unimodally distributed with no clear evidence for a discrete dimorphism. Mixture analyses did not reveal evidence of a discrete or even strong dimorphism. These results raise doubts about previous claims, as reported in textbooks, that head variation in P. microlepis represents a discrete dimorphism of left- and right-bending forms. Based on extensive field sampling that excluded ambiguous (i.e. symmetric or weakly asymmetric) individual adults, we found that left and right morphs occur in equal abundance in five populations. Moreover, mate pairing for 51 wild-caught pairs was random with regard to head laterality, calling into question reports that this laterality is maintained through disassortative mating.
PMCID: PMC3497103  PMID: 23055070
behavioural laterality; Lake Tanganyika; mixture analysis; negative frequency-dependent selection; Perissodus microlepis; random mating
8.  Retinoic Acid Is Involved in the Metamorphosis of the Anal Fin into an Intromittent Organ, the Gonopodium, in the Green Swordtail (Xiphophorus hellerii) 
PLoS ONE  2013;8(10):e77580.
In poeciliid fish the male anal fin has been transformed into a gonopodium, an intromittent organ required for internal fertilization. Elevated testosterone levels induce metamorphosis of a subset of anal fin rays to grow and form the specialized terminal structures of the gonopodium. The molecular mechanisms underlying these processes are largely unknown. Here, we investigated whether retinoic acid (RA) signaling is involved in gonopodium development in the swordtail Xiphophorus hellerii. We showed that aldh1a2, a RA synthesizing enzyme, and the RA receptors, rar-ga and rar-gb, are expressed in anal fins during metamorphosis. aldh1a2 expression is regulated by testosterone in a concentration-dependent manner and is up-regulated in both hormone-induced and naturally developing gonopodia. Androgen receptor (ar), a putative regulator of gonopodial development, is co-expressed with aldh1a2 and the RA receptors in gonopodial rays. Importantly, experimental increase of RA signaling promoted growth of the gonopodium and increased the number of new segments. Based on gene expression analyses and pharmacological manipulation of gonopodium development, we show that the RA signaling pathway is activated in response to androgen signaling and promotes fin ray growth and development during the metamorphosis of the anal fin into the gonopodium.
PMCID: PMC3808415  PMID: 24204880
9.  Analysis of the African coelacanth genome sheds light on tetrapod evolution 
Amemiya, Chris T. | Alföldi, Jessica | Lee, Alison P. | Fan, Shaohua | Philippe, Hervé | MacCallum, Iain | Braasch, Ingo | Manousaki, Tereza | Schneider, Igor | Rohner, Nicolas | Organ, Chris | Chalopin, Domitille | Smith, Jeramiah J. | Robinson, Mark | Dorrington, Rosemary A. | Gerdol, Marco | Aken, Bronwen | Biscotti, Maria Assunta | Barucca, Marco | Baurain, Denis | Berlin, Aaron M. | Blatch, Gregory L. | Buonocore, Francesco | Burmester, Thorsten | Campbell, Michael S. | Canapa, Adriana | Cannon, John P. | Christoffels, Alan | De Moro, Gianluca | Edkins, Adrienne L. | Fan, Lin | Fausto, Anna Maria | Feiner, Nathalie | Forconi, Mariko | Gamieldien, Junaid | Gnerre, Sante | Gnirke, Andreas | Goldstone, Jared V. | Haerty, Wilfried | Hahn, Mark E. | Hesse, Uljana | Hoffmann, Steve | Johnson, Jeremy | Karchner, Sibel I. | Kuraku, Shigehiro | Lara, Marcia | Levin, Joshua Z. | Litman, Gary W. | Mauceli, Evan | Miyake, Tsutomu | Mueller, M. Gail | Nelson, David R. | Nitsche, Anne | Olmo, Ettore | Ota, Tatsuya | Pallavicini, Alberto | Panji, Sumir | Picone, Barbara | Ponting, Chris P. | Prohaska, Sonja J. | Przybylski, Dariusz | Saha, Nil Ratan | Ravi, Vydianathan | Ribeiro, Filipe J. | Sauka-Spengler, Tatjana | Scapigliati, Giuseppe | Searle, Stephen M. J. | Sharpe, Ted | Simakov, Oleg | Stadler, Peter F. | Stegeman, John J. | Sumiyama, Kenta | Tabbaa, Diana | Tafer, Hakim | Turner-Maier, Jason | van Heusden, Peter | White, Simon | Williams, Louise | Yandell, Mark | Brinkmann, Henner | Volff, Jean-Nicolas | Tabin, Clifford J. | Shubin, Neil | Schartl, Manfred | Jaffe, David | Postlethwait, John H. | Venkatesh, Byrappa | Di Palma, Federica | Lander, Eric S. | Meyer, Axel | Lindblad-Toh, Kerstin
Nature  2013;496(7445):311-316.
It was a zoological sensation when a living specimen of the coelacanth was first discovered in 1938, as this lineage of lobe-finned fish was thought to have gone extinct 70 million years ago. The modern coelacanth looks remarkably similar to many of its ancient relatives, and its evolutionary proximity to our own fish ancestors provides a glimpse of the fish that first walked on land. Here we report the genome sequence of the African coelacanth, Latimeria chalumnae. Through a phylogenomic analysis, we conclude that the lungfish, and not the coelacanth, is the closest living relative of tetrapods. Coelacanth protein-coding genes are significantly more slowly evolving than those of tetrapods, unlike other genomic features . Analyses of changes in genes and regulatory elements during the vertebrate adaptation to land highlight genes involved in immunity, nitrogen excretion and the development of fins, tail, ear, eye, brain, and olfaction. Functional assays of enhancers involved in the fin-to-limb transition and in the emergence of extra-embryonic tissues demonstrate the importance of the coelacanth genome as a blueprint for understanding tetrapod evolution.
PMCID: PMC3633110  PMID: 23598338
10.  Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution 
Nature genetics  2013;45(4):415-421e2.
Lampreys are representatives of an ancient vertebrate lineage that diverged from our own ~500 million years ago. By virtue of this deeply shared ancestry, the sea lamprey (P. marinus) genome is uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology. Here, we present the first lamprey whole-genome sequence and assembly. We note challenges faced owing to its high content of repetitive elements and GC bases, as well as the absence of broad-scale sequence information from closely related species. Analyses of the assembly indicate that two whole-genome duplications likely occurred before the divergence of ancestral lamprey and gnathostome lineages. Moreover, the results help define key evolutionary events within vertebrate lineages, including the origin of myelin-associated proteins and the development of appendages. The lamprey genome provides an important resource for reconstructing vertebrate origins and the evolutionary events that have shaped the genomes of extant organisms.
PMCID: PMC3709584  PMID: 23435085
11.  Resampling-Based Approaches to Study Variation in Morphological Modularity 
PLoS ONE  2013;8(7):e69376.
Modularity has been suggested to be connected to evolvability because a higher degree of independence among parts allows them to evolve as separate units. Recently, the Escoufier RV coefficient has been proposed as a measure of the degree of integration between modules in multivariate morphometric datasets. However, it has been shown, using randomly simulated datasets, that the value of the RV coefficient depends on sample size. Also, so far there is no statistical test for the difference in the RV coefficient between a priori defined groups of observations. Here, we (1), using a rarefaction analysis, show that the value of the RV coefficient depends on sample size also in real geometric morphometric datasets; (2) propose a permutation procedure to test for the difference in the RV coefficient between a priori defined groups of observations; (3) show, through simulations, that such a permutation procedure has an appropriate Type I error; (4) suggest that a rarefaction procedure could be used to obtain sample-size-corrected values of the RV coefficient; and (5) propose a nearest-neighbor procedure that could be used when studying the variation of modularity in geographic space. The approaches outlined here, readily extendable to non-morphometric datasets, allow study of the variation in the degree of integration between a priori defined modules. A Java application – that will allow performance of the proposed test using a software with graphical user interface – has also been developed and is available at the Morphometrics at Stony Brook Web page (
PMCID: PMC3712944  PMID: 23874956
12.  Saltatory Evolution of the Ectodermal Neural Cortex Gene Family at the Vertebrate Origin 
Genome Biology and Evolution  2013;5(8):1485-1502.
The ectodermal neural cortex (ENC) gene family, whose members are implicated in neurogenesis, is part of the kelch repeat superfamily. To date, ENC genes have been identified only in osteichthyans, although other kelch repeat-containing genes are prevalent throughout bilaterians. The lack of elaborate molecular phylogenetic analysis with exhaustive taxon sampling has obscured the possible link of the establishment of this gene family with vertebrate novelties. In this study, we identified ENC homologs in diverse vertebrates by means of database mining and polymerase chain reaction screens. Our analysis revealed that the ENC3 ortholog was lost in the basal eutherian lineage through single-gene deletion and that the triplication between ENC1, -2, and -3 occurred early in vertebrate evolution. Including our original data on the catshark and the zebrafish, our comparison revealed high conservation of the pleiotropic expression pattern of ENC1 and shuffling of expression domains between ENC1, -2, and -3. Compared with many other gene families including developmental key regulators, the ENC gene family is unique in that conventional molecular phylogenetic inference could identify no obvious invertebrate ortholog. This suggests a composite nature of the vertebrate-specific gene repertoire, consisting not only of de novo genes introduced at the vertebrate origin but also of long-standing genes with no apparent invertebrate orthologs. Some of the latter, including the ENC gene family, may be too rapidly evolving to provide sufficient phylogenetic signals marking orthology to their invertebrate counterparts. Such gene families that experienced saltatory evolution likely remain to be explored and might also have contributed to phenotypic evolution of vertebrates.
PMCID: PMC3762194  PMID: 23843192
vertebrate novelty; saltation; gene loss; conserved synteny; whole genome duplication
13.  Revealing Less Derived Nature of Cartilaginous Fish Genomes with Their Evolutionary Time Scale Inferred with Nuclear Genes 
PLoS ONE  2013;8(6):e66400.
Cartilaginous fishes, divided into Holocephali (chimaeras) and Elasmoblanchii (sharks, rays and skates), occupy a key phylogenetic position among extant vertebrates in reconstructing their evolutionary processes. Their accurate evolutionary time scale is indispensable for better understanding of the relationship between phenotypic and molecular evolution of cartilaginous fishes. However, our current knowledge on the time scale of cartilaginous fish evolution largely relies on estimates using mitochondrial DNA sequences. In this study, making the best use of the still partial, but large-scale sequencing data of cartilaginous fish species, we estimate the divergence times between the major cartilaginous fish lineages employing nuclear genes. By rigorous orthology assessment based on available genomic and transcriptomic sequence resources for cartilaginous fishes, we selected 20 protein-coding genes in the nuclear genome, spanning 2973 amino acid residues. Our analysis based on the Bayesian inference resulted in the mean divergence time of 421 Ma, the late Silurian, for the Holocephali-Elasmobranchii split, and 306 Ma, the late Carboniferous, for the split between sharks and rays/skates. By applying these results and other documented divergence times, we measured the relative evolutionary rate of the Hox A cluster sequences in the cartilaginous fish lineages, which resulted in a lower substitution rate with a factor of at least 2.4 in comparison to tetrapod lineages. The obtained time scale enables mapping phenotypic and molecular changes in a quantitative framework. It is of great interest to corroborate the less derived nature of cartilaginous fish at the molecular level as a genome-wide phenomenon.
PMCID: PMC3692497  PMID: 23825540
14.  Transcriptomics of morphological color change in polychromatic Midas cichlids 
BMC Genomics  2013;14:171.
Animal pigmentation has received much attention in evolutionary biology research due to its strong implications for adaptation and speciation. However, apart from a few cases the genetic changes associated with these evolutionary processes remain largely unknown. The Midas cichlid fish from Central America are an ideal model system for investigating pigmentation traits that may also play a role in speciation. Most Midas cichlids maintain their melanophores and exhibit a grayish (normal) color pattern throughout their lives. A minority of individuals, however, undergo color change and exhibit a distinctive gold or even white coloration in adulthood. The ontogenetic color change in the Midas cichlids may also shed light on the molecular mechanisms underlying pigmentation disorders in humans.
Here we use next-generation sequencing (Illumina) RNAseq analyses to compare skin transcriptome-wide expression levels in three distinct stages of color transformation in Midas cichlids. cDNA libraries of scale tissue, for six biological replicates of each group, were generated and sequenced using Illumina technology. Using a combination of three differential expression (DE) analyses we identified 46 candidate genes that showed DE between the color morphs. We find evidence for two key DE patterns: a) genes involved in melanosomal pathways are up-regulated in normally pigmented fish; and b) immediate early and inflammatory response genes were up-regulated in transitional fish, a response that parallels some human skin disorders such as melanoma formation and psoriasis. One of the DE genes segregates with the gold phenotype in a genetic cross and might be associated with incipient speciation in this highly “species-rich” lineage of cichlids.
Using transcriptomic analyses we successfully identified key expression differences between different color morphs of Midas cichlid fish. These differentially expressed genes have important implications for our understanding of the molecular mechanisms underlying speciation in this lineage of extremely young species since they mate strongly assortatively, and new species may arise by sexual selection due to this color polymorphism. Some of the human orthologues of the genes identified here may also be involved in pigmentation differences and diseases and therefore provide genetic markers for the detection of human pigmentation disorders.
PMCID: PMC3623868  PMID: 23497064
RNAseq; Color change; Melanophore; Differential expression; Tyrosinase genes; Midas cichlids
15.  Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and Neotropical lineages 
Cichlid fishes are remarkably phenotypically diverse and species-rich. Therefore, they provide an exciting opportunity for the study of the genetics of adaptation and speciation by natural and sexual selection. Here, we review advances in the genomics and transcriptomics of cichlids, particularly regarding ecologically relevant differences in body shape, trophic apparatus, coloration and patterning, and sex determination. Research conducted so far has focused almost exclusively on African cichlids. To analyse genomic diversity and selection in a Neotropical radiation, we conducted a comparative transcriptomic analysis between sympatric, ecologically divergent crater-lake Midas cichlids (Lake Xiloá Amphilophus amarillo and Amphilophus sagittae). We pyrosequenced (Roche 454) expressed sequence tag (EST) libraries and generated more than 178 000 000 ESTs and identified nine ESTs under positive selection between these sister species (Ka/Ks > 1). None of these ESTs were found to be under selection in African cichlids. Of 11 candidate genes for ecomorphological differentiation in African cichlids, none showed signs of selection between A. amarillo and A. sagittae. Although more population-level studies are now needed to thoroughly document patterns of divergence during speciation of cichlids, available information so far suggests that adaptive phenotypic diversification in Neotropical and African cichlids may be evolving through non-parallel genetic bases.
PMCID: PMC3233715  PMID: 22201168
next-generation sequencing; cichlid fish; ecological speciation; coloration; body shape; expressed sequence tags
16.  Comprehensive phylogenetic analysis of all species of swordtails and platies (Pisces: Genus Xiphophorus) uncovers a hybrid origin of a swordtail fish, Xiphophorus monticolus, and demonstrates that the sexually selected sword originated in the ancestral lineage of the genus, but was lost again secondarily 
Males in some species of the genus Xiphophorus, small freshwater fishes from Meso-America, have an extended caudal fin, or sword – hence their common name “swordtails”. Longer swords are preferred by females from both sworded and – surprisingly also, non-sworded (platyfish) species that belong to the same genus. Swordtails have been studied widely as models in research on sexual selection. Specifically, the pre-existing bias hypothesis was interpreted to best explain the observed bias of females in presumed ancestral lineages of swordless species that show a preference for assumed derived males with swords over their conspecific swordless males. However, many of the phylogenetic relationships within this genus still remained unresolved. Here we construct a comprehensive molecular phylogeny of all 26 known Xiphophorus species, including the four recently described species (X. kallmani, X. mayae, X. mixei and X. monticolus). We use two mitochondrial and six new nuclear markers in an effort to increase the understanding of the evolutionary relationships among the species in this genus. Based on the phylogeny, the evolutionary history and character state evolution of the sword was reconstructed and found to have originated in the common ancestral lineage of the genus Xiphophorus and that it was lost again secondarily.
We estimated the evolutionary relationships among all known species of the genus Xiphophorus based on the largest set of DNA markers so far. The phylogeny indicates that one of the newly described swordtail species, Xiphophorus monticolus, is likely to have arisen through hybridization since it is placed with the southern platyfish in the mitochondrial phylogeny, but with the southern swordtails in the nuclear phylogeny. Such discordance between these two types of markers is a strong indication for a hybrid origin. Additionally, by using a maximum likelihood approach the possession of the sexually selected sword trait is shown to be the most likely ancestral state for the genus Xiphophorus. Further, we provide a well supported estimation of the phylogenetic relationships between the previously unresolved northern swordtail groups.
This comprehensive molecular phylogeny of the entire genus Xiphophorus provides evidence that a second swordtail species, X. monticolus, arose through hybridization. Previously, we demonstrated that X. clemenciae, another southern swordtail species, arose via hybridization. These findings highlight the potential key role of hybridization in the evolution of this genus and suggest the need for further investigations into how hybridization contributes to speciation more generally.
PMCID: PMC3585855  PMID: 23360326
17.  Trade-offs in cavefish sensory capacity 
BMC Biology  2013;11:5.
In caves one repeatedly finds strikingly convergent patterns of evolution in diverse sets of organisms involving 'regressive' traits such as the loss of eyes and pigmentation. Ongoing debate centers around whether these regressive traits arise as the result of neutral evolutionary processes, or rather by natural selection of 'constructive' traits that arise at the expense of eyes and pigmentation. Recent research on cavefish points to the latter, suggesting that the 'constructive' trait vibrational attractive behavior and the reduction of eye size may share a common genetic basis.
See research article
PMCID: PMC3554488  PMID: 23347449
18.  A Hybrid Genetic Linkage Map of Two Ecologically and Morphologically Divergent Midas Cichlid Fishes (Amphilophus spp.) Obtained by Massively Parallel DNA Sequencing (ddRADSeq) 
G3: Genes|Genomes|Genetics  2013;3(1):65-74.
Cichlid fishes are an excellent model system for studying speciation and the formation of adaptive radiations because of their tremendous species richness and astonishing phenotypic diversity. Most research has focused on African rift lake fishes, although Neotropical cichlid species display much variability as well. Almost one dozen species of the Midas cichlid species complex (Amphilophus spp.) have been described so far and have formed repeated adaptive radiations in several Nicaraguan crater lakes. Here we apply double-digest restriction-site associated DNA sequencing to obtain a high-density linkage map of an interspecific cross between the benthic Amphilophus astorquii and the limnetic Amphilophus zaliosus, which are sympatric species endemic to Crater Lake Apoyo, Nicaragua. A total of 755 RAD markers were genotyped in 343 F2 hybrids. The map resolved 25 linkage groups and spans a total distance of 1427 cM with an average marker spacing distance of 1.95 cM, almost matching the total number of chromosomes (n = 24) in these species. Regions of segregation distortion were identified in five linkage groups. Based on the pedigree of parents to F2 offspring, we calculated a genome-wide mutation rate of 6.6 × 10−8 mutations per nucleotide per generation. This genetic map will facilitate the mapping of ecomorphologically relevant adaptive traits in the repeated phenotypes that evolved within the Midas cichlid lineage and, as the first linkage map of a Neotropical cichlid, facilitate comparative genomic analyses between African cichlids, Neotropical cichlids and other teleost fishes.
PMCID: PMC3538344  PMID: 23316439
Midas cichlid; double-digest RADSeq; synteny; segregation distortion; RAD markers; mutation rate
19.  Handed Foraging Behavior in Scale-Eating Cichlid Fish: Its Potential Role in Shaping Morphological Asymmetry 
PLoS ONE  2012;7(9):e44670.
Scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika display handed (lateralized) foraging behavior, where an asymmetric ‘left’ mouth morph preferentially feeds on the scales of the right side of its victim fish and a ‘right’ morph bites the scales of the left side. This species has therefore become a textbook example of the astonishing degree of ecological specialization and negative frequency-dependent selection. We investigated the strength of handedness of foraging behavior as well as its interaction with morphological mouth laterality in P. microlepis. In wild-caught adult fish we found that mouth laterality is, as expected, a strong predictor of their preferred attack orientation. Also laboratory-reared juvenile fish exhibited a strong laterality in behavioral preference to feed on scales, even at an early age, although the initial level of mouth asymmetry appeared to be small. This suggests that pronounced mouth asymmetry is not a prerequisite for handed foraging behavior in juvenile scale-eating cichlid fish and might suggest that behavioral preference to attack a particular side of the prey plays a role in facilitating morphological asymmetry of this species.
PMCID: PMC3435272  PMID: 22970282
20.  Eggspot Number and Sexual Selection in the Cichlid Fish Astatotilapia burtoni 
PLoS ONE  2012;7(8):e43695.
Sexual selection on male coloration is one of the main mechanisms proposed to explain the explosive speciation rates in East African cichlid fish. True eggspots are color patterns characteristic of the most species-rich lineage of cichlids, the Haplochromini, and have been suggested to be causally related to the speciation processes. Eggspots are thought to have originated by sensory exploitation and subsequently gained several roles in sexual advertisement. However, for most of these functions the evidence is equivocal. In addition, the genetic architecture of this trait still is largely unknown. We conducted bidirectional selective breeding experiments for eggspot numbers in the model cichlid, Astatotilapia burtoni. After two generations, low lines responded significantly, whereas the high lines did not. Body size was both phenotypically and genotypically correlated with eggspot number and showed correlated response to selection. Males with higher numbers of eggspots were found to sire larger offspring. Despite the potential to act as honest indicators of fitness, the behavioral experiments showed no evidence of a role in either intra- or inter-sexual selection. Visual-based female preference was instead explained by courtship intensity. The evolution of this trait has been interpreted in light of adaptive theories of sexual selection, however the present and published results suggest the influence of non-adaptive factors such as sensory exploitation, environmental constraints and sexual antagonism.
PMCID: PMC3427294  PMID: 22937082
21.  Horizontal Transfers of Tc1 Elements between Teleost Fishes and Their Vertebrate Parasites, Lampreys 
Genome Biology and Evolution  2012;4(9):929-936.
Horizontal gene transfer (HGT) has been recognized to be an important mechanism that shaped the evolution and genomes of prokaryotes and unicellular eukaryotes. However, HGT is regarded to be exceedingly rare among eukaryotes. We discovered massive transfers of a DNA transposon, a Tc1 element encoding a transposase, between multiple teleost fishes and lampreys that last shared a common ancestor over 500 Ma. Members of this group of Tc1 elements were found to exhibit a mosaic phylogenetic distribution, yet their sequences were highly similar even between distantly related lineages (95%–99% identity). Our molecular phylogenetic analyses suggested that horizontal transfers of this element happened repeatedly, involving multiple teleost fishes that are phylogenetically only distantly related. Interestingly, almost all the affected teleost lineages are also known to be subject to lamprey parasitism, suggesting that the horizontal transfers between vertebrates might have occurred through parasite–host interaction. The genomes of several northern hemisphere lamprey species, including that of the sea lamprey (Petromyzon marinus), were found to contain thousands of copies of the foreign elements. Impact of this event is discussed in relation to other peculiar genomic features of lampreys.
PMCID: PMC3516227  PMID: 22887124
lamprey; Salmonidae; Tc1 transposase; horizontal gene transfer
22.  Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni 
Cichlid fishes are a textbook example of rapid speciation and exuberant diversity—this applies especially to haplochromines, a lineage with approximately 1800 species. Haplochromine males uniquely possess oval, bright spots on their anal fin, called ‘egg-spots’ or ‘egg-dummies’. These are presumed to be an evolutionary key innovation that contributed to the tribe's evolutionary success. Egg-spots have been proposed to mimic the ova of the mouthbrooding females of the corresponding species, contribute to fertilization success and even facilitate species recognition. Interestingly, egg-spot number varies extensively not only between species, but also within some populations. This high degree of intraspecific variation may appear to be counterintuitive since selection might be expected to act to stabilize traits that are correlated with fitness measures. We addressed this ‘paradox’ experimentally, and found that in the haplochromine cichlid Astatotilapia burtoni, the number of egg-spots was related to male age, body condition and dominance status. Intriguingly, the egg-spot number also had a high heritable component (narrow sense heritability of 0.5). These results suggest that the function of egg-spots might have less to do with fertilization success or species recognition, but rather relate to mate choice and/or male–male competition, helping to explain the high variability in this important trait.
PMCID: PMC3119019  PMID: 21208958
body condition; dominance hierarchy; narrow sense heritability; intraspecific variation; key innovation; signal value
24.  Cyclohexane-1,2-Dione Hydrolase from Denitrifying Azoarcus sp. Strain 22Lin, a Novel Member of the Thiamine Diphosphate Enzyme Family▿† 
Journal of Bacteriology  2011;193(23):6760-6769.
Alicyclic compounds with hydroxyl groups represent common structures in numerous natural compounds, such as terpenes and steroids. Their degradation by microorganisms in the absence of dioxygen may involve a C—C bond ring cleavage to form an aliphatic intermediate that can be further oxidized. The cyclohexane-1,2-dione hydrolase (CDH) (EC from denitrifying Azoarcus sp. strain 22Lin, grown on cyclohexane-1,2-diol as a sole electron donor and carbon source, is the first thiamine diphosphate (ThDP)-dependent enzyme characterized to date that cleaves a cyclic aliphatic compound. The degradation of cyclohexane-1,2-dione (CDO) to 6-oxohexanoate comprises the cleavage of a C—C bond adjacent to a carbonyl group, a typical feature of reactions catalyzed by ThDP-dependent enzymes. In the subsequent NAD+-dependent reaction, 6-oxohexanoate is oxidized to adipate. CDH has been purified to homogeneity by the criteria of gel electrophoresis (a single band at ∼59 kDa; calculated molecular mass, 64.5 kDa); in solution, the enzyme is a homodimer (∼105 kDa; gel filtration). As isolated, CDH contains 0.8 ± 0.05 ThDP, 1.0 ± 0.02 Mg2+, and 1.0 ± 0.015 flavin adenine dinucleotide (FAD) per monomer as a second organic cofactor, the role of which remains unclear. Strong reductants, Ti(III)-citrate, Na+-dithionite, and the photochemical 5-deazaflavin/oxalate system, led to a partial reduction of the FAD chromophore. The cleavage product of CDO, 6-oxohexanoate, was also a substrate; the corresponding cyclic 1,3- and 1,4-diones did not react with CDH, nor did the cis- and trans-cyclohexane diols. The enzymes acetohydroxyacid synthase (AHAS) from Saccharomyces cerevisiae, pyruvate oxidase (POX) from Lactobacillus plantarum, benzoylformate decarboxylase from Pseudomonas putida, and pyruvate decarboxylase from Zymomonas mobilis were identified as the closest relatives of CDH by comparative amino acid sequence analysis, and a ThDP binding motif and a 2-fold Rossmann fold for FAD binding could be localized at the C-terminal end and central region of CDH, respectively. A first mechanism for the ring cleavage of CDO is presented, and it is suggested that the FAD cofactor in CDH is an evolutionary relict.
PMCID: PMC3232874  PMID: 21965568
25.  Introduced Predator Elicits Deficient Brood Defence Behaviour in a Crater Lake Fish 
PLoS ONE  2012;7(1):e30064.
Introduced species represent one of the most serious global threats to biodiversity. In this field-based study, we assessed behavioural responses of brood tending cichlid fish to an invasive predator of their offspring. This was achieved by comparing parental defence responses of the endangered arrow cichlid (Amphilophus zaliosus), a fish species endemic to the crater lake Apoyo in Nicaragua, towards the bigmouth sleeper (Gobiomorus dormitor), a formidable predator of cichlid fry, and all other potential fish predators of offspring. The bigmouth sleeper was recently introduced into Apoyo but naturally co-exists with cichlids in a few other Nicaraguan lakes. Arrow cichlid parents allowed bigmouth sleepers to advance much closer to their fry than other predators before initiating aggressive brood defence behaviours. Interestingly, parents of a very closely related species, A. sagittae, which has coevolved with bigmouth sleepers in crater lake Xiloá, reacted to approaching bigmouth sleepers at comparable distances as to other predators of cichlid fry. These results provide a novel demonstration of the specific mechanism (i.e. naive parental behaviour) by which invasive predators may negatively affect species that lack the adequate behavioural repertoire.
PMCID: PMC3253807  PMID: 22253881

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