Jeanne M. Serb

Molecular phylogenetics of the Pectinidae (Mollusca: Bivalvia) and effect of increased taxon sampling and outgroup selection on tree topology

Evolutionary relationships of the Pectinidae were examined using two mitochondrial genes (12S rRNA, 16S rRNA) and one nuclear gene (Histone H3) for 46 species. Outgroup taxa from Propeamussidae, Spondylidae and Limidae were also sequenced to examine the impact of outgroup choice on pectinid topologies. Our phylogenetic analyses resolved the Pectinidae as monophyletic, but many of the subfamilies and tribes within the family do not form monophyletic clades. The paraphyletic Aequipectinini group is the most basal member of the Pectinidae, with the Chlamydinae and Palliolinae representing the most recently derived pectinid groups. These results are in contrast with the current morphological hypothesis of Pectinidae evolution, which suggests the Chlamydinae and Pallioline are basal groups within the Pectinidae. Ingroup topology was found to be sensitive to outgroup choice and increasing taxon sampling within the Pectinidae resulted in more robust phylogenies.

Convergent and parallel evolution in life habit of the scallops (Bivalvia: Pectinidae)

BackgroundWe employed a phylogenetic framework to identify patterns of life habit evolution in the marine bivalve family Pectinidae. Specifically, we examined the number of independent origins of each life habit and distinguished between convergent and parallel trajectories of life habit evolution using ancestral state estimation. We also investigated whether ancestral character states influence the frequency or type of evolutionary trajectories.ResultsWe determined that temporary attachment to substrata by byssal threads is the most likely ancestral condition for the Pectinidae, with subsequent transitions to the five remaining habit types. Nearly all transitions between life habit classes were repeated in our phylogeny and the majority of these transitions were the result of parallel evolution from byssate ancestors. Convergent evolution also occurred within the Pectinidae and produced two additional gliding clades and two recessing lineages. Furthermore, our analysis indicates that byssal attaching gave rise to significantly more of the transitions than any other life habit and that the cementing and nestling classes are only represented as evolutionary outcomes in our phylogeny, never as progenitor states.ConclusionsCollectively, our results illustrate that both convergence and parallelism generated repeated life habit states in the scallops. Bias in the types of habit transitions observed may indicate constraints due to physical or ontogenetic limitations of particular phenotypes.

Gene duplication and the origins of morphological complexity in pancrustacean eyes, a genomic approach

BackgroundDuplication and divergence of genes and genetic networks is hypothesized to be a major driver of the evolution of complexity and novel features. Here, we examine the history of genes and genetic networks in the context of eye evolution by using new approaches to understand patterns of gene duplication during the evolution of metazoan genomes. We hypothesize that 1) genes involved in eye development and phototransduction have duplicated and are retained at higher rates in animal clades that possess more distinct types of optical design; and 2) genes with functional relationships were duplicated and lost together, thereby preserving genetic networks. To test these hypotheses, we examine the rates and patterns of gene duplication and loss evident in 19 metazoan genomes, including that of Daphnia pulex - the first completely sequenced crustacean genome. This is of particular interest because the pancrustaceans (hexapods+crustaceans) have more optical designs than any other major clade of animals, allowing us to test specifically whether the high amount of disparity in pancrustacean eyes is correlated with a higher rate of duplication and retention of vision genes.ResultsUsing protein predictions from 19 metazoan whole-genome projects, we found all members of 23 gene families known to be involved in eye development or phototransduction and deduced their phylogenetic relationships. This allowed us to estimate the number and timing of gene duplication and loss events in these gene families during animal evolution. When comparing duplication/retention rates of these genes, we found that the rate was significantly higher in pancrustaceans than in either vertebrates or non-pancrustacean protostomes. Comparing patterns of co-duplication across Metazoa showed that while these eye-genes co-duplicate at a significantly higher rate than those within a randomly shuffled matrix, many genes with known functional relationships in model organisms did not co-duplicate more often than expected by chance.ConclusionsOverall, and when accounting for factors such as differential rates of whole-genome duplication in different groups, our results are broadly consistent with the hypothesis that genes involved in eye development and phototransduction duplicate at a higher rate in Pancrustacea, the group with the greatest variety of optical designs. The result that these genes have a significantly high number of co-duplications and co-losses could be influenced by shared functions or other unstudied factors such as synteny. Since we did not observe co-duplication/co-loss of genes for all known functional modules (e.g. specific regulatory networks), the interactions among suites of known co-functioning genes (modules) may be plastic at the temporal scale of analysis performed here. Other factors in addition to gene duplication - such as cis-regulation, heterotopy, and co-option - are also likely to be strong factors in the diversification of eye types.

Identification of 'extinct' freshwater mussel species using DNA barcoding

Freshwater mollusks are highly imperiled, with 70% of the North American species extinct, endangered, or at risk of extinction. Impoundments and other human impacts on the Coosa River of Alabama, Georgia and Tennessee of the southeastern USA alone are believed to have caused 50 mollusk species extinctions, but uncertainty over boundaries among several putatively closely related species makes this number preliminary. Our examination of freshwater mussels collected during an extensive survey of the upper‐drainage basin, DNA barcoding and molecular phylogenetic analyses confirm the rediscovery of four morphospecies in the genus Pleurobema (Unionidae) previously thought to be extinct from the upper Coosa basin. A fifth ‘extinct’ form was found in an adjoining basin. Molecular data show that the Coosa morphologies represent at least three species‐level taxa: Pleurobema decisum, P. hanleyianum and P. stabile. Endemism is higher than currently recognized, both at the species level and for multispecies clades. Prompt conservation efforts may preserve some of these taxa and their ecosystem.

Using phylogenetically-informed annotation (PIA) to search for light-interacting genes in transcriptomes from non-model organisms

BackgroundTools for high throughput sequencing and de novo assembly make the analysis of transcriptomes (i.e. the suite of genes expressed in a tissue) feasible for almost any organism. Yet a challenge for biologists is that it can be difficult to assign identities to gene sequences, especially from non-model organisms. Phylogenetic analyses are one useful method for assigning identities to these sequences, but such methods tend to be time-consuming because of the need to re-calculate trees for every gene of interest and each time a new data set is analyzed. In response, we employed existing tools for phylogenetic analysis to produce a computationally efficient, tree-based approach for annotating transcriptomes or new genomes that we term Phylogenetically-Informed Annotation (PIA), which places uncharacterized genes into pre-calculated phylogenies of gene families.ResultsWe generated maximum likelihood trees for 109 genes from a Light Interaction Toolkit (LIT), a collection of genes that underlie the function or development of light-interacting structures in metazoans. To do so, we searched protein sequences predicted from 29 fully-sequenced genomes and built trees using tools for phylogenetic analysis in the Osiris package of Galaxy (an open-source workflow management system). Next, to rapidly annotate transcriptomes from organisms that lack sequenced genomes, we repurposed a maximum likelihood-based Evolutionary Placement Algorithm (implemented in RAxML) to place sequences of potential LIT genes on to our pre-calculated gene trees. Finally, we implemented PIA in Galaxy and used it to search for LIT genes in 28 newly-sequenced transcriptomes from the light-interacting tissues of a range of cephalopod mollusks, arthropods, and cubozoan cnidarians. Our new trees for LIT genes are available on the Bitbucket public repository (http://bitbucket.org/osiris_phylogenetics/pia/) and we demonstrate PIA on a publicly-accessible web server (http://galaxy-dev.cnsi.ucsb.edu/pia/).ConclusionsOur new trees for LIT genes will be a valuable resource for researchers studying the evolution of eyes or other light-interacting structures. We also introduce PIA, a high throughput method for using phylogenetic relationships to identify LIT genes in transcriptomes from non-model organisms. With simple modifications, our methods may be used to search for different sets of genes or to annotate data sets from taxa outside of Metazoa.

The last common ancestor of most bilaterian animals possessed at least 9 opsins.

Abstract The opsin gene family encodes key proteins animals use to sense light and has expanded dramatically as it originated early in animal evolution. Understanding the origins of opsin diversity can offer clues to how separate lineages of animals have repurposed different opsin paralogs for different light-detecting functions. However, the more we look for opsins outside of eyes and from additional animal phyla, the more opsins we uncover, suggesting we still do not know the true extent of opsin diversity, nor the ancestry of opsin diversity in animals. To estimate the number of opsin paralogs present in both the last common ancestor of the Nephrozoa (bilaterians excluding Xenoacoelomorpha), and the ancestor of Cnidaria + Bilateria, we reconstructed a reconciled opsin phylogeny using sequences from 14 animal phyla, especially the traditionally poorly-sampled echinoderms and molluscs. Our analysis strongly supports a repertoire of at least nine opsin paralogs in the bilaterian ancestor and at least four opsin paralogs in the last common ancestor of Cnidaria + Bilateria. Thus, the kernels of extant opsin diversity arose much earlier in animal history than previously known. Further, opsins likely duplicated and were lost many times, with different lineages of animals maintaining different repertoires of opsin paralogs. This phylogenetic information can inform hypotheses about the functions of different opsin paralogs and can be used to understand how and when opsins were incorporated into complex traits like eyes and extraocular sensors.

De Novo Assembly and Characterization of Two Transcriptomes Reveal Multiple Light-Mediated Functions in the Scallop Eye (Bivalvia: Pectinidae)

Background The eye has evolved across 13 separate lineages of molluscs. Yet, there have been very few studies examining the molecular machinary underlying eye function of this group, which is due, in part, to a lack of genomic resources. The scallop (Bivalvia: Pectinidae) represents a compeling molluscan model to study photoreception due to its morphologically novel and separately evolved mirror-type eye. We sequenced the adult eye transcriptome of two scallop species to: 1) identify the phototransduction pathway components; 2) identify any additional light detection functions; and 3) test the hypothesis that molluscs possess genes not found in other animal lineages. Results A total of 3,039 contigs from the bay scallop, Argopecten irradians and 26,395 contigs from the sea scallop, Placopecten magellanicus were produced by 454 sequencing. Targeted BLAST searches and functional annotation using Gene Ontology (GO) terms and KEGG pathways identified transcripts from three light detection systems: two phototransduction pathways and the circadian clock, a previously unrecognized function of the scallop eye. By comparing the scallop transcriptomes to molluscan and non-molluscan genomes, we discovered that a large proportion of the transcripts (7,776 sequences) may be specific to the scallop lineage. Nearly one-third of these contain transmembrane protein domains, suggesting these unannotated transcripts may be sensory receptors. Conclusions Our data provide the most comprehensive transcriptomic resource currently available from a single molluscan eye type. Candidate genes potentially involved in sensory reception were identified, and are worthy of further investigation. This resource, combined with recent phylogenetic and genomic data, provides a strong foundation for future investigations of the function and evolution of molluscan photosensory systems in this morphologically and taxonomically diverse phylum.

Rates of molecular evolution vary in vertebrates for insulin-like growth factor-1 (IGF-1), a pleiotropic locus that regulates life history traits.

Insulin-like growth factor-1 (IGF-1) is a member of the vertebrate insulin/insulin-like growth factor/relaxin gene family necessary for growth, reproduction, and survival at both the cellular and organismal level. Its sequence, protein structure, and function have been characterized in mammals, birds, and fish; however, a notable gap in our current knowledge of the function of IGF-1 and its molecular evolution is information in ectothermic reptiles. To address this disparity, we sequenced the coding region of IGF-1 in 11 reptile species-one crocodilian, three turtles, three lizards, and four snakes. Complete sequencing of the full mRNA transcript of a snake revealed the Ea-isoform, the predominant isoform of IGF-1 also reported in other vertebrate groups. A gene tree of the IGF-1 protein-coding region that incorporated sequences from diverse vertebrate groups showed similarity to the species phylogeny, with the exception of the placement of Testudines as sister group to Aves, due to their high nucleotide sequence similarity. In contrast, long-branch lengths indicate more rapid divergence in IGF-1 among lizards and snakes. Additionally, lepidosaurs (i.e., lizards and snakes) had higher rates of non-synonymous:synonymous substitutions (dN/dS) relative to archosaurs (i.e., birds and crocodilians) and turtles. Tests for positive selection on specific codons within branches and evaluation of the changes in the amino acid properties, suggested positive selection in lepidosaurs on the C domain of IGF-1, which is involved in binding affinity to the IGF-1 receptor. Predicted structural changes suggest that major alterations in protein structure and function may have occurred in reptiles. These data propose new insights into the molecular co-evolution of IGF-1 and its receptors, and ultimately the evolution of IGF-1s role in regulating life-history traits across vertebrates.

Congruence and Conflict Between Molecular and Reproductive Characters When Assessing Biological Diversity in the Western Fanshell Cyprogenia aberti (Bivalvia, Unionidae)

Abstract Organisms with complex life histories and unusual modes of genome inheritance can present challenges for phylogenetic reconstruction and accurate assessment of biological diversity. This is particularly true for freshwater bivalves in the family Unionidae because: (1) they have complex life cycles that include a parasitic larva and obligate fish host; (2) they possess both a male and female mitochondrial genome that is transmitted through doubly uniparental inheritance (DUI); and (3) they are found in riverine habitats with complex hydrogeological histories. Examination of mitochondrial DNA (mtDNA) sequences, conglutinate morphology, and host fish compatibility of the western fanshell Cyprogenia aberti (Conrad, 1850) revealed significant character variation across its range. Although variation was correlated among the different data sets and supports discrete groups, these groups did not always correspond to geographically isolated populations. Two discrete mtDNA clades exist sympatrically within most C. aberti populations, and these same clades are also diagnosed by at least one morphological character, egg color. The surprisingly high genetic distance (14.61%–20.19%) between the members of these sympatric clades suggests heritance infidelity of the two different mitochondrial genomes. This hypothesis was tested and falsified. More general patterns in geography were observed in host fish compatibility. Populations of C. aberti from the major river systems differed in their ability to utilize fish species as hosts. These differences in reproductive traits, which are presumably genetically based, suggest that these populations are not ecologically exchangeable with one another and represent biological diversity not previously recognized within Cyprogenia Agassiz, 1852.

Trends in the sand: directional evolution in the shell shape of recessing scallops (Bivalvia: Pectinidae)

Directional evolution is one of the most compelling evolutionary patterns observed in macroevolution. Yet, despite its importance, detecting such trends in multivariate data remains a challenge. In this study, we evaluate multivariate evolution of shell shape in 93 bivalved scallop species, combining geometric morphometrics and phylogenetic comparative methods. Phylomorphospace visualization described the history of morphological diversification in the group; revealing that taxa with a recessing life habit were the most distinctive in shell shape, and appeared to display a directional trend. To evaluate this hypothesis empirically, we extended existing methods by characterizing the mean directional evolution in phylomorphospace for recessing scallops. We then compared this pattern to what was expected under several alternative evolutionary scenarios using phylogenetic simulations. The observed pattern did not fall within the distribution obtained under multivariate Brownian motion, enabling us to reject this evolutionary scenario. By contrast, the observed pattern was more similar to, and fell within, the distribution obtained from simulations using Brownian motion combined with a directional trend. Thus, the observed data are consistent with a pattern of directional evolution for this lineage of recessing scallops. We discuss this putative directional evolutionary trend in terms of its potential adaptive role in exploiting novel habitats.