Molecular evolution of opsins, a gene responsible for sensing light, in scallops (Bivalvia: Pectinidae)

Genetic diversity can cause drastic effects on phenotypes and is commonly the result of a gene duplication event. Gene duplication and subsequent functional divergence of opsins, a G-protein coupled-receptor (GPCR), have played an important role in expanding photoreceptive capabilities of organisms by altering what wavelengths of light are absorbed by photoreceptors (spectral tuning). Relatively few studies have been devoted to exploring the role of opsin duplication and evolution in non-arthropod invertebrates, and even fewer have integrated all the potential genetic diversity of opsins. In this dissertation, I utilized the photosensory system of the scallop, a marine bivalve, to study the evolution and expansion of the genetically diverse opsins, and demonstrate the complicated nature of Gq-opsin diversification after gene duplication. First, I explored how opsin paralogs diversify in function and evolutionary fate by characterizing four rhabdomeric (Gq-protein coupled) opsins in the scallop, Argopecten irradians. Using a phylogenetic framework, I showed a pattern consistent with two rounds of duplication generating the four paralogous Gq-opsins in scallops. Differential expression of the four Gq-opsins across ocular and extra-ocular photosensitive tissues suggested that the Gq-opsins are used in different biological contexts in scallops, while protein modeling reveals variation in the amino acid composition, suggesting the four Gq-opsin paralogs may absorb different wavelengths of light. Second, I investigated how two Gq-opsin paralogs differentiate after a duplication event across the scallop family, Pectinidae. By comparing the rates of evolution between paralogous clades, I demonstrated both paralogs are under purifying selection, yet maintained at rates that are significantly different. I showed that one amino acid position, which is not considered a putative spectral tuning site, stands out as a strong candidate to explain the source of selection driving the difference in evolutionary rates. Finally, I discussed the current role of allelic variation in sensory systems and described how alleles are often discarded in studies of molecular evolution. I demonstrated the breadth of possible allelic variation within an individual and stressed the potential of cryptic genetic variation in the evolution of organisms by examining the allelic variation in Gq-opsins sampled across 34 bivalve species

Structural differences and differential expression among rhabdomeric opsins reveal functional change after gene duplication in the bay scallop, Argopecten irradians (Pectinidae)

Background Opsins are the only class of proteins used for light perception in image-forming eyes. Gene duplication and subsequent functional divergence of opsins have played an important role in expanding photoreceptive capabilities of organisms by altering what wavelengths of light are absorbed by photoreceptors (spectral tuning). However, new opsin copies may also acquire novel function or subdivide ancestral functions through changes to temporal, spatial or the level of gene expression. Here, we test how opsin gene copies diversify in function and evolutionary fate by characterizing four rhabdomeric (Gq-protein coupled) opsins in the scallop, Argopecten irradians, identified from tissue-specific transcriptomes. Results Under a phylogenetic analysis, we recovered a pattern consistent with two rounds of duplication that generated the genetic diversity of scallop Gq-opsins. We found strong support for differential expression of paralogous Gq-opsins across ocular and extra-ocular photosensitive tissues, suggesting that scallop Gq-opsins are used in different biological contexts due to molecular alternations outside and within the protein-coding regions. Finally, we used available protein models to predict which amino acid residues interact with the light-absorbing chromophore. Variation in these residues suggests that the four Gq-opsin paralogs absorb different wavelengths of light. Conclusions Our results uncover novel genetic and functional diversity in the light-sensing structures of the scallop, demonstrating the complicated nature of Gq-opsin diversification after gene duplication. Our results highlight a change in the nearly ubiquitous shadow response in molluscs to a narrowed functional specificity for visual processes in the eyed scallop. Our findings provide a starting point to study how gene duplication may coincide with eye evolution, and more specifically, different ways neofunctionalization of Gq-opsins may occur

Molecular phylogeny of the Pectinoidea (Bivalvia) indicates Propeamussiidae to be a non-monophyletic family with one clade sister to the scallops (Pectinidae)

Scallops (Pectinidae) are one of the most diverse families of bivalves and have been a model system in evolutionary biology. However, in order to understand phenotypic evolution, the Pectinidae needs to be placed in a deeper phylogenetic framework within the superfamily Pectinoidea. We reconstructed a molecular phylogeny for 60 species from four of the five extant families within the Pectinoidea using a five gene dataset (12S, 16S, 18S, 28S rRNAs and histone H3). Our analyses give consistent support for the non-monophyly of the Propeamussiidae, with a subset of species as the sister group to the Pectinidae, the Propeamussiidae type species as sister to the Spondylidae, and the majority of propeamussiid taxa sister to the Spondylidae + Pr. dalli. This topology represents a previously undescribed relationship of pectinoidean families. Our results suggest a single origin for eyes within the superfamily and likely multiple instances of loss for these characters. However, it is now evident that reconstructing the evolutionary relationships of Pectinoidea will require a more comprehensive taxonomic sampling of the Propeamussiidae sensu lato

Book Review of: 'Relevance theory : recent developments, current challenges and future directions' by M. Padilla Cruz (ed.)

Gq-opsin sequences included in the phylogenetic analysis. Asterisks represent sequences obtained through Porter et al. [27]. For additional information regarding sequence acquisition not available on Genbank, see supplementary material in Porter et al. [27]. (DOCX 25 kb

Herbivory and nutrients shape grassland soil seed banks

Anthropogenic nutrient enrichment and shifts in herbivory can lead to dramatic changes in the composition and diversity of aboveground plant communities. In turn, this can alter seed banks in the soil, which are cryptic reservoirs of plant diversity. Here, we use data from seven Nutrient Network grassland sites on four continents, encompassing a range of climatic and environmental conditions, to test the joint effects of fertilization and aboveground mammalian herbivory on seed banks and on the similarity between aboveground plant communities and seed banks. We find that fertilization decreases plant species richness and diversity in seed banks, and homogenizes composition between aboveground and seed bank communities. Fertilization increases seed bank abundance especially in the presence of herbivores, while this effect is smaller in the absence of herbivores. Our findings highlight that nutrient enrichment can weaken a diversity maintaining mechanism in grasslands, and that herbivory needs to be considered when assessing nutrient enrichment effects on seed bank abundance.EEA Santa CruzFil: Eskelinen, Anu. German Centre for Integrative Biodiversity Research; AlemaniaFil: Eskelinen, Anu. Helmholtz Centre for Environmental Research. Department of Physiological Diversity; AlemaniaFil: Eskelinen, Anu. University of Oulu. Ecology & Genetics; FinlandiaFil: Jessen, Maria Theresa. Helmholtz Centre for Environmental Research. Department of Physiological Diversity; AlemaniaFil: Jessen, Maria Theresa. German Centre for Integrative Biodiversity Research; AlemaniaFil: Jessen, Maria Theresa. Helmholtz Centre for Environmental Research – UFZ. Department of Community Ecology; AlemaniaFil: Bahamonde, Hector Alejandro. Universidad Nacional de La Plata. Ciencias Agrarias y Forestales; Argentina.Fil: Bakker, Jonathan D. University of Washington. School of Environmental and Forest Sciences; Estados UnidosFil: Borer, Elizabeth T. University of Minnesota. Department of Ecology, Evolution & Behavior; Estados UnidosFil: Caldeira, Maria C. University of Lisbon. Forest Research Centre. Associate Laboratory TERRA. School of Agriculture; Portugal.Fil: Harpole, William Stanley. German Centre for Integrative Biodiversity Research (iDiv); AlemaniaFil: Harpole, William Stanley. Helmholtz Centre for Environmental Research – UFZ. Department of Community Ecology; AlemaniaFil: Harpole, William Stanley. Martin Luther University. Institute of Biology; AlemaniaFil: Jia, Meiyu. University of Washington. School of Environmental and Forest Sciences; Estados UnidosFil: Jia, Meiyu. East China University of Technology. School of Water Resources & Environmental Engineering; China.Fil: Jia, Meiyu. Beijing Normal University. College of Life Sciences; China.Fil: Lannes, Luciola S. São Paulo State University-UNESP. Department of Biology and Animal Sciences; Brasil.Fil: Nogueira, Carla. University of Lisbon. Forest Research Centre. Associate Laboratory TERRA. School of Agriculture; Portugal.Fil: Venterink, Harry Olde. Vrije Universiteit Brussel (VUB). Department of Biology; BélgicaFil: Peri, Pablo Luis. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Santa Cruz; Argentina.Fil: Peri, Pablo Luis. Universidad Nacional de la Patagonia Austral; Argentina.Fil: Peri, Pablo Luis. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina.Fil: Porath-Krause, Anita J. University of Minnesota. Department of Ecology, Evolution & Behavior; Estados UnidosFil: Seabloom, Eric William. University of Minnesota. Department of Ecology, Evolution & Behavior; Estados UnidosFil: Schroeder, Katie. University of Minnesota. Department of Ecology, Evolution & Behavior; Estados UnidosFil: Schroeder, Katie. University of Georgia. Odum School of Ecology; Estados UnidosFil: Tognetti, Pedro M. Universidad de Buenos Aires. Facultad de Agronomía; Argentina.Fil: Tognetti, Pedro M. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura (IFEVA); Argentina.Fil: Tognetti, Pedro M. Swiss Federal Institute for Forest, Snow and Landscape Research WSL; SuizaFil: Yasui, Simone-Louise E. Queensland University of Technology. School of Biological and Environmental Sciences; Australia.Fil: Virtanen, Risto. University of Oulu. Ecology & Genetics; FinlandiaFil: Sullivan, Lauren L. University of Missouri. Division of Biological Sciences; Estados UnidosFil: Sullivan, Lauren L. Michigan State University. Department of Plant Biology; Estados UnidosFil: Sullivan, Lauren L. Michigan State University. W. K. Kellogg Biological Station; Estados UnidosFil: Sullivan, Lauren L. Michigan State University. Ecology, Evolution and Behavior Program; Estados Unido

Molecular evolution of opsins, a gene responsible for sensing light, in scallops (Bivalvia: Pectinidae)

Genetic diversity can cause drastic effects on phenotypes and is commonly the result of a gene duplication event. Gene duplication and subsequent functional divergence of opsins, a G-protein coupled-receptor (GPCR), have played an important role in expanding photoreceptive capabilities of organisms by altering what wavelengths of light are absorbed by photoreceptors (spectral tuning). Relatively few studies have been devoted to exploring the role of opsin duplication and evolution in non-arthropod invertebrates, and even fewer have integrated all the potential genetic diversity of opsins. In this dissertation, I utilized the photosensory system of the scallop, a marine bivalve, to study the evolution and expansion of the genetically diverse opsins, and demonstrate the complicated nature of Gq-opsin diversification after gene duplication. First, I explored how opsin paralogs diversify in function and evolutionary fate by characterizing four rhabdomeric (Gq-protein coupled) opsins in the scallop, Argopecten irradians. Using a phylogenetic framework, I showed a pattern consistent with two rounds of duplication generating the four paralogous Gq-opsins in scallops. Differential expression of the four Gq-opsins across ocular and extra-ocular photosensitive tissues suggested that the Gq-opsins are used in different biological contexts in scallops, while protein modeling reveals variation in the amino acid composition, suggesting the four Gq-opsin paralogs may absorb different wavelengths of light. Second, I investigated how two Gq-opsin paralogs differentiate after a duplication event across the scallop family, Pectinidae. By comparing the rates of evolution between paralogous clades, I demonstrated both paralogs are under purifying selection, yet maintained at rates that are significantly different. I showed that one amino acid position, which is not considered a putative spectral tuning site, stands out as a strong candidate to explain the source of selection driving the difference in evolutionary rates. Finally, I discussed the current role of allelic variation in sensory systems and described how alleles are often discarded in studies of molecular evolution. I demonstrated the breadth of possible allelic variation within an individual and stressed the potential of cryptic genetic variation in the evolution of organisms by examining the allelic variation in Gq-opsins sampled across 34 bivalve species.</p

Aphids increase leaf fungal endophyte diversity and abundance across a plant community regardless of viral infection status and plant nutrition

Faculty adviser: Elizabeth BorerBarley/cereal yellow dwarf viruses (B/CYDVs) are an important group of aphid-vectored viruses that infect grasses worldwide. The virus is transmitted from plant to plant when aphids feed on infected plants and then disperse and feed on uninfected hosts. In this process, aphids likely transfer bacterial and fungal endophytes from the plant microbiome among plants, however, this has not been directly tested. Fungal endophytes provide host plants with protection from herbivores and protect plants against abiotic stressors like drought and nutrient stress. Plant nutrient content shapes aphid feeding preference, the effect of viral infections on plants and increases aphid abundance. Previous work conducted within the lab showed that viral infection in the aphids changed their feeding behaviors. Infected aphids had higher dispersal from host plants and had increased preference for uninfected plants. Thus, we hypothesized that aphids would move fungal endophytes among plants within a neighborhood, however, fertilization and aphids with the virus would increase movement of endophytes among plants. To explore these hypotheses, we constructed plant communities by placing 100 barley plants within a 10 x 10 grid which were fully enclosed within a sealed enclosure to create replicate plant communities. We added aphids (C/BYDV infected, uninfected, or no aphids) to the center plants within each of the enclosures. Half of the plant communities were randomly selected to receive a fertilization treatment (0.2% or 10% of half-strength Hoagland’s solution). Over the next four months, we randomly harvested plants from each ring of the 10 x 10 grid bi-weekly. We collected ~0.5g of plant leaf tissue, and plated ground leaf tissue on malt extract agar (MEA) petri plate to isolate fungal endophytes from leaf tissue. After 1 week of growth, we identified and enumerated all fungal taxa growing on the plates. Overall, we found that the presence of aphid vectors increase the diversity (F = 73.86, p = 0.0001), abundance (F = 6.512, p = 0.0028) of fungal endophyte communities, however we found that viral status (Turkey’s diff = -0.502, p = 0.144), plant nutrient status (diversity: F1,59 = 1.91, p = 0.173, abundance: F1,59 = 1.49, p = 0.227), and location (diversity: F3,59 = 1.09, p = 0.361, abundance: F3,59 = 0.626, p = 0.601) of the plants within our plant community had no effect on endophyte diversity or abundance. We performed a PERMANOVA analysis to determine how aphid presence, viral status, fertilization, and location in the plant community shaped endophyte community composition using both abundance-weighted Bray-Curtis distance and presence/absence-weighted Jaccard’s distance. We found that the presence of aphids (BC: r2 = 0.202, p = 0.01) and fertilizer addition (BC: r2 = 0.020, p = 0.05) as well as their interaction (BC: r2 = 0.023, p = 0.01) weakly but significantly altered fungal community composition with both Bray-Curtis and Jaccard’s distance. Our results demonstrate that aphids alter the diversity, abundance, and which fungal taxa are present within barley leaves, while plant nutrient content changes what taxa are in barley leaves without altering the overall diversity or abundance of fungal taxa.This research was supported by the Undergraduate Research Opportunities Program (UROP)

Structural differences and differential expression among rhabdomeric opsins reveal functional change after gene duplication in the bay scallop, Argopecten irradians (Pectinidae)

Background Opsins are the only class of proteins used for light perception in image-forming eyes. Gene duplication and subsequent functional divergence of opsins have played an important role in expanding photoreceptive capabilities of organisms by altering what wavelengths of light are absorbed by photoreceptors (spectral tuning). However, new opsin copies may also acquire novel function or subdivide ancestral functions through changes to temporal, spatial or the level of gene expression. Here, we test how opsin gene copies diversify in function and evolutionary fate by characterizing four rhabdomeric (Gq-protein coupled) opsins in the scallop, Argopecten irradians, identified from tissue-specific transcriptomes. Results Under a phylogenetic analysis, we recovered a pattern consistent with two rounds of duplication that generated the genetic diversity of scallop Gq-opsins. We found strong support for differential expression of paralogous Gq-opsins across ocular and extra-ocular photosensitive tissues, suggesting that scallop Gq-opsins are used in different biological contexts due to molecular alternations outside and within the protein-coding regions. Finally, we used available protein models to predict which amino acid residues interact with the light-absorbing chromophore. Variation in these residues suggests that the four Gq-opsin paralogs absorb different wavelengths of light. Conclusions Our results uncover novel genetic and functional diversity in the light-sensing structures of the scallop, demonstrating the complicated nature of Gq-opsin diversification after gene duplication. Our results highlight a change in the nearly ubiquitous shadow response in molluscs to a narrowed functional specificity for visual processes in the eyed scallop. Our findings provide a starting point to study how gene duplication may coincide with eye evolution, and more specifically, different ways neofunctionalization of Gq-opsins may occur.This article is published as Porath-Krause, Anita J., Autum N. Pairett, Davide Faggionato, Bhagyashree S. Birla, Kannan Sankar, and Jeanne M. Serb. "Structural differences and differential expression among rhabdomeric opsins reveal functional change after gene duplication in the bay scallop, Argopecten irradians (Pectinidae)." BMC evolutionary biology 16, no. 1 (2016): 250. doi: 10.1186/s12862-016-0823-9. Posted with permission.</p

annual_perennial_tissue

Preference data for annual versus perennial tissues of aphids (R. padi) that are non-viruliferous versus viruliferous