Despite contingency in life's history, the similarity of evolutionarily convergent traits may represent predictable solutions to common conditions. However, the extent to which overall gene expression levels (transcriptomes) underlying convergent traits are themselves convergent remains largely unexplored. Here, we show strong statistical support for convergent evolutionary origins and massively parallel evolution of the entire transcriptomes in symbiotic bioluminescent organs (bacterial photophores) from two divergent squid species. The gene expression similarities are so strong that regression models of one species' photophore can predict organ identity of a distantly related photophore from gene expression levels alone. Our results point to widespread parallel changes in gene expression evolution associated with convergent origins of complex organs. Therefore, predictable solutions may drive not only the evolution of novel, complex organs but also the evolution of overall gene expression levels that underlie them.

Montastraea cavernosa is a common coral in the Caribbean basin found in several color morphs. To investigate the causes for brown and orange morphs we undertook a genomics approach on corals collected at the same time and depth in the Bahamas. The coral holobiont includes the host, symbiotic dinoflagellates (Symbiodinium spp.), and a diverse microbiome. While the coral host showed significant genetic differentiation between color morphs both the composition of the Symbiodinium spp. communities and the prokaryotic communities did not. Both targeted and global gene expression differences in the transcriptome of the host show no difference in fluorescent proteins while the metatranscriptome of the microbiome shows that pigments such as phycoerythrin and orange carotenoid protein of cyanobacterial origin are significantly greater in orange morphs, which is also consistent with the significantly greater number of cyanobacteria quantified by 16S rRNA reads and flow cytometry. The microbiome of orange color morphs expressed significantly more nitrogenase (nifH) transcripts consistent with their known ability to fix nitrogen. Both coral and Symbiodinium spp. transcriptomes from orange morphs had significantly increased expression of genes related to immune response and apoptosis, which may potentially be involved in maintaining and regulating the unique symbiont population in orange morphs.

Abstract Background Duplication 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. Results Using 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. Conclusions Overall, 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.

Resurveys of historical collecting localities have revealed range shifts, primarily leading edge expansions, which have been attributed to global warming. However, there have been few spatially replicated community-scale resurveys testing whether species' responses are spatially consistent. Here we repeated early twentieth century surveys of small mammals along elevational gradients in northern, central and southern regions of montane California. Of the 34 species we analysed, 25 shifted their ranges upslope or downslope in at least one region. However, two-thirds of ranges in the three regions remained stable at one or both elevational limits and none of the 22 species found in all three regions shifted both their upper and lower limits in the same direction in all regions. When shifts occurred, high-elevation species typically contracted their lower limits upslope, whereas low-elevation species had heterogeneous responses. For high-elevation species, site-specific change in temperature better predicted the direction of shifts than change in precipitation, whereas the direction of shifts by low-elevation species was unpredictable by temperature or precipitation. While our results support previous findings of primarily upslope shifts in montane species, they also highlight the degree to which the responses of individual species vary across geographically replicated landscapes.

Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative-fitness-based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best-studied mutualisms. We find that although there are numerous observations of low-quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative-fitness-based definition of cheating.

Background

Tools 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.

Results

We 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/ ).

Conclusions

Our 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.