Julia C. Jones

Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes

Crater lakes provide a natural laboratory to study speciation of cichlid fishes by ecological divergence. Up to now, there has been a dearth of transcriptomic and genomic information that would aid in understanding the molecular basis of the phenotypic differentiation between young species. We used next‐generation sequencing (Roche 454 massively parallel pyrosequencing) to characterize the diversity of expressed sequence tags between ecologically divergent, endemic and sympatric species of cichlid fishes from crater lake Apoyo, Nicaragua: benthic Amphilophus astorquii and limnetic Amphilophus zaliosus. We obtained 24 174 A. astorquii and 21 382 A. zaliosus high‐quality expressed sequence tag contigs, of which 13 106 pairs are orthologous between species. Based on the ratio of nonsynonymous to synonymous substitutions, we identified six sequences exhibiting signals of strong diversifying selection (Ka/Ks > 1). These included genes involved in biosynthesis, metabolic processes and development. This transcriptome sequence variation may be reflective of natural selection acting on the genomes of these young, sympatric sister species. Based on Ks ratios and p‐distances between 3′‐untranslated regions (UTRs) calibrated to previously published species divergence times, we estimated a neutral transcriptome‐wide substitutional mutation rate of ∼1.25 × 10−6 per site per year. We conclude that next‐generation sequencing technologies allow us to infer natural selection acting to diversify the genomes of young species, such as crater lake cichlids, with much greater scope than previously possible.

The evolutionary history of Xiphophorus fish and their sexually selected sword: a genome-wide approach using restriction site-associated DNA sequencing.

Next‐generation sequencing (NGS) techniques are now key tools in the detection of population genomic and gene expression differences in a large array of organisms. However, so far few studies have utilized such data for phylogenetic estimations. Here, we use NGS data obtained from genome‐wide restriction site‐associated DNA (RAD) (∼66000 SNPs) to estimate the phylogenetic relationships among all 26 species of swordtail and platyfish (genus Xiphophorus) from Central America. Past studies, both sequence and morphology‐based, have differed in their inferences of the evolutionary relationships within this genus, particularly at the species‐level and among monophyletic groupings. We show that using a large number of markers throughout the genome, we are able to infer the phylogenetic relationships with unparalleled resolution for this genus. The relationships among all three major clades and species within each of them are highly resolved and consistent under maximum likelihood, Bayesian inference and maximum parsimony. However, we also highlight the current cautions with this data type and analyses. This genus exhibits a particularly interesting evolutionary history where at least two species may have arisen through hybridization events. Here, we are able to infer the paternal lineages of these putative hybrid species. Using the RAD‐marker‐based tree we reconstruct the evolutionary history of the sexually selected sword trait and show that it may have been present in the common ancestor of the genus. Together our results highlight the outstanding capacity that RAD sequencing data has for resolving previously problematic phylogenetic relationships, particularly among relatively closely related species.

Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes

Determining the genetic bases of adaptations and their roles in speciation is a prominent issue in evolutionary biology. Cichlid fish species flocks are a prime example of recent rapid radiations, often associated with adaptive phenotypic divergence from a common ancestor within a short period of time. In several radiations of freshwater fishes, divergence in ecomorphological traits — including body shape, colour, lips and jaws — is thought to underlie their ecological differentiation, specialization and, ultimately, speciation. The Midas cichlid species complex (Amphilophus spp.) of Nicaragua provides one of the few known examples of sympatric speciation where species have rapidly evolved different but parallel morphologies in young crater lakes. This study identified significant QTL for body shape using SNPs generated via ddRAD sequencing and geometric morphometric analyses of a cross between two ecologically and morphologically divergent, sympatric cichlid species endemic to crater Lake Apoyo: an elongated limnetic species (Amphilophus zaliosus) and a high‐bodied benthic species (Amphilophus astorquii). A total of 453 genome‐wide informative SNPs were identified in 240 F2 hybrids. These markers were used to construct a genetic map in which 25 linkage groups were resolved. Seventy‐two segregating SNPs were linked to 11 QTL. By annotating the two most highly supported QTL‐linked genomic regions, genes that might contribute to divergence in body shape along the benthic–limnetic axis in Midas cichlid sympatric adaptive radiations were identified. These results suggest that few genomic regions of large effect contribute to early stage divergence in Midas cichlids.

DNA Methylation Mediates the Discriminatory Power of Associative Long-Term Memory in Honeybees

Memory is created by several interlinked processes in the brain, some of which require long-term gene regulation. Epigenetic mechanisms are likely candidates for regulating memory-related genes. Among these, DNA methylation is known to be a long lasting genomic mark and may be involved in the establishment of long-term memory. Here we demonstrate that DNA methyltransferases, which induce and maintain DNA methylation, are involved in a particular aspect of associative long-term memory formation in honeybees, but are not required for short-term memory formation. While long-term memory strength itself was not affected by blocking DNA methyltransferases, odor specificity of the memory (memory discriminatory power) was. Conversely, perceptual discriminatory power was normal. These results suggest that different genetic pathways are involved in mediating the strength and discriminatory power of associative odor memories and provide, to our knowledge, the first indication that DNA methyltransferases are involved in stimulus-specific associative long-term memory formation.

Transcriptomics of morphological color change in polychromatic Midas cichlids

BackgroundAnimal 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.ResultsHere 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.ConclusionsUsing 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.

The gut microbial community of midas cichlid fish in repeatedly evolved limnetic-benthic species pairs

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.

Genetic support for random mating between left and right‐mouth morphs in the dimorphic scale‐eating cichlid fish Perissodus microlepis from Lake Tanganyika

Population genetic analyses were conducted to investigate whether random mating occurs between left and right-mouth morphs of the dimorphic scale-eating cichlid fish Perissodus microlepis from two geographical sites in southern Lake Tanganyika. The mitochondrial and nuclear DNA markers (13 microsatellite loci) revealed no genetic differentiation between left and right morphs (i.e. widespread interbreeding). The observed lack of genetic divergence between the different morphs allowed for the exclusion of the possibility of assortative mating between same morph types. The microsatellite data showed no significant departures of heterozygosity from Hardy-Weinberg equilibrium, suggesting purely random mating between the morphs. Overall, this study indicated no genetic evidence for either assortative or disassortative mating, but it did provide support for the random mating hypothesis. Highly significant, albeit weak, spatial population structure was also found when samples of different morphs were pooled according to geographical sites. An additional analysis of two microsatellite loci that were recently suggested to be putatively linked to the genetic locus that determines the laterality of these mouth morphs did not show any such association.

A phylogeographic investigation of the hybrid origin of a species of swordtail fish from Mexico.

Hybrid speciation may contribute significantly to generating biodiversity, but only a few well‐documented examples for it exist so far that do not involve polyploidization as a mechanism. The swordtail fish, Xiphophorus clemenciae, shows common hallmarks of a hybrid origin and still overlaps in its current geographic distribution with its putative ancestral species (Xiphophorus hellerii and Xiphophorus maculatus). Xiphophorus clemenciae provides an ideal system for investigating the possible continued genetic interactions between a hybrid and its parental species. Here, we use microsatellite and mitochondrial markers to investigate the population structure of these species of swordtails and search for signs of recent hybridization. Individuals were sampled from 21 localities across the known range of X. clemenciae– the Isthmus of Tehuantepec (IT) Mexico, and several environmental parameters that might represent barriers to dispersal were recorded. The hybridization event that gave rise to X. clemenciae appears to be rather ancient, and a single origin is likely. We find negligible evidence for ongoing hybridization and introgression between the putative ancestral species, because they now occupy distinct ecological niches, and a common haplotype is shared by most populations of X. clemenciae. The population structure within these species shows an isolation‐by‐distance (IBD) pattern and genetic differentiation between most populations is significant and high. We infer that tectonic evolution in the Isthmus has greatly restricted gene flow between the southern and central IT populations of X. clemenciae and X. helleriii and provide preliminary information to aid in conservation management of this geographically restricted hybrid species, X. clemenciae.

Evolution of the elaborate male intromittent organ of Xiphophorus fishes

Abstract Internally fertilizing animals show a remarkable diversity in male genital morphology that is associated with sexual selection, and these traits are thought to be evolving particularly rapidly. Male fish in some internally fertilizing species have “gonopodia,” highly modified anal fins that are putatively important for sexual selection. However, our understanding of the evolution of genital diversity remains incomplete. Contrary to the prediction that male genital traits evolve more rapidly than other traits, here we show that gonopodial traits and other nongonopodial traits exhibit similar evolutionary rates of trait change and also follow similar evolutionary models in an iconic genus of poeciliid fish (Xiphophorus spp.). Furthermore, we find that both mating and nonmating natural selection mechanisms are unlikely to be driving the diverse Xiphophorus gonopodial morphology. Putative holdfast features of the male genital organ do not appear to be influenced by water flow, a candidate selective force in aquatic habitats. Additionally, interspecific divergence in gonopodial morphology is not significantly higher between sympatric species, than between allopatric species, suggesting that male genitals have not undergone reproductive character displacement. Slower rates of evolution in gonopodial traits compared with a subset of putatively sexually selected nongenital traits suggest that different selection mechanisms may be acting on the different trait types. Further investigations of this elaborate trait are imperative to determine whether it is ultimately an important driver of speciation.

Will he still look good with the lights on? Spectral tuning of visual pigments in fish

Visual perception is a key element in evolution, as it is required for many life processes. Two recent studies in BMC Biology and BMC Evolutionary Biology shed light on the genetic determinants of color detection in strikingly colored fish.