Plastic and evolved responses to global change: What can we learn from comparative transcriptomics?

© The American Genetic Association. 2015. All rights reserved. Physiological plasticity and adaptive evolution may facilitate persistence in a changing environment. As a result, there is an interest in understanding species\u27 capacities for plastic and evolved responses, and the mechanisms by which these responses occur. Transcriptome sequencing has become a powerful tool for addressing these questions, providing insight into otherwise unobserved effects of changing conditions on organismal physiology and variation in these effects among individuals and populations. Here, we review recent studies using comparative transcriptomics to understand plastic and evolutionary responses to changing environments. We focus on 2 areas where transcriptomics has played an important role: first, in understanding the genetic basis for local adaptation to current gradients as a proxy for future adaptation, and second, in understanding organismal responses to multiple stressors. We find most studies examining multiple stressors have tested the effects of each stressor individually; the few studies testing multiple stressors simultaneously have found synergistic effects on gene expression that would not have been predicted from single stressor studies. We discuss the importance of robust experimental design to allow for a more sophisticated characterization of transcriptomic responses and conclude by offering recommendations for future research, including integrating genomics with transcriptomics, testing gene regulatory networks, and comparing the equivalence of transcription to translation and the effects of environmental stress on the proteome

Evaluating summary statistics used to test for incomplete lineage sorting: Mito-nuclear discordance in the reef sponge Callyspongia vaginalis

Conflicting patterns of population differentiation between the mitochondrial and nuclear genomes (mito-nuclear discordance) have become increasingly evident as multilocus data sets have become easier to generate. Incomplete lineage sorting (ILS) of nucDNA is often implicated as the cause of such discordance, stemming from the large effective population size of nucDNA relative to mtDNA. However, selection, sex-biased dispersal and historical demography can also lead to mito-nuclear discordance. Here, we compare patterns of genetic diversity and subdivision for six nuclear protein-coding gene regions to those for mtDNA in a common Caribbean coral reef sponge, Callyspongia vaginalis, along the Florida reef tract. We also evaluated a suite of summary statistics to determine which are effective metrics for comparing empirical and simulated data when testing drivers of mito-nuclear discordance in a statistical framework. While earlier work revealed three divergent and geographically subdivided mtDNACOI haplotypes separated by 2.4% sequence divergence, nuclear alleles were admixed with respect to mitochondrial clade and geography. Bayesian analysis showed that substitution rates for the nuclear loci were up to 7 times faster than for mitochondrial COI. Coalescent simulations and neutrality tests suggested that mito-nuclear discordance in C. vaginalis is not the result of ILS in the nucDNA or selection on the mtDNA but is more likely caused by changes in population size. Sperm-mediated gene flow may also influence patterns of population subdivision in the nucDNA. © 2013 John Wiley & Sons Ltd

Host and Symbionts in Pocillopora damicornis Larvae Display Different Transcriptomic Responses to Ocean Acidification and Warming

As global ocean change progresses, reef-building corals and their early life history stages will rely on physiological plasticity to tolerate new environmental conditions. Larvae from brooding coral species contain algal symbionts upon release, which assist with the energy requirements of dispersal and metamorphosis. Global ocean change threatens the success of larval dispersal and settlement by challenging the performance of the larvae and of the symbiosis. In this study, larvae of the reef-building coral Pocillopora damicornis were exposed to elevated pCO2 and temperature to examine the performance of the coral and its symbionts in situ and better understand the mechanisms of physiological plasticity and stress tolerance in response to multiple stressors. We generated a de novo holobiont transcriptome containing coral host and algal symbiont transcripts and bioinformatically filtered the assembly into host and symbiont components for downstream analyses. Seventeen coral genes were differentially expressed in response to the combined effects of pCO2 and temperature. In the symbiont, 89 genes were differentially expressed in response to pCO2. Our results indicate that many of the whole-organism (holobiont) responses previously observed for P. damicornis larvae in scenarios of ocean acidification and warming may reflect the physiological capacity of larvae to cope with the environmental changes without expressing additional protective mechanisms. At the holobiont level, the results suggest that the responses of symbionts to future ocean conditions could play a large role in shaping success of coral larval stages

Genetic Connectivity in The Branching Vase Sponge (callyspongia Vaginalis) Across The Florida Reef Tract And Caribbean

The Porifera constitute a substantial fraction of the biomass on coral reefs and frequently have higher species diversity than corals and algae, making this phylum an important model for the investigation of reef connectivity. We examined genetic connectivity in the common branching vase sponge, Callyspongia vaginalis, by analyzing DNA sequence variation in 511 bp of the mitochondrial cytochrome oxidase I (COI) gene in 401 individuals sampled from 16 locations throughout the Florida reef tract and Caribbean. Populations of Callyspongia vaginalis were highly genetically structured over the study area (ΦST = 0.48, P \u3c 0.0001), including over distances as short as tens of kilometers within the Florida reef tract, and had a significant overall pattern of isolation by distance (P = 0.0002). However, nonsignificant pairwise ΦST values were also found between a few Florida sampling sites suggesting that long distance dispersal, perhaps by means of fragmentation, may occur over continuous, shallow coastlines. Indeed, sufficient gene flow appears to occur along the Florida reef tract to obscure a signal of isolation by distance (P = 0.164), but not to homogenize haplotype frequencies over 465 km from Palm Beach to the Dry Tortugas. Statistical parsimony analysis revealed two highly divergent haplotypes from Honduras suggestive of cryptic speciation. Inferences from a nested clade analysis supported the pattern of restricted gene flow and isolation by distance in the Caribbean, and suggested a northward range extension of C. vaginalis from a hypothesized Central American ancestral population into the Gulf of Mexico and Florida. The extensive genetic structuring in this common reef sponge is consistent with expectations based on typically short sponge larval durations, suggesting that sponge recruitment to coral reefs may be largely local source driven

Variable levels of drift in tunicate cardiopharyngeal gene regulatory elements.

Background: Mutations in gene regulatory networks often lead to genetic divergence without impacting gene expression or developmental patterning. The rules governing this process of developmental systems drift, including the variable impact of selective constraints on different nodes in a gene regulatory network, remain poorly delineated. Results: Here we examine developmental systems drift within the cardiopharyngeal gene regulatory networks of two tunicate species, Corella inflata and Ciona robusta. Cross-species analysis of regulatory elements suggests that trans-regulatory architecture is largely conserved between these highly divergent species. In contrast, cis-regulatory elements within this network exhibit distinct levels of conservation. In particular, while most of the regulatory elements we analyzed showed extensive rearrangements of functional binding sites, the enhancer for the cardiopharyngeal transcription factor FoxF is remarkably well-conserved. Even minor alterations in spacing between binding sites lead to loss of FoxF enhancer function, suggesting that bound trans-factors form position-dependent complexes. Conclusions: Our findings reveal heterogeneous levels of divergence across cardiopharyngeal cis-regulatory elements. These distinct levels of divergence presumably reflect constraints that are not clearly associated with gene function or position within the regulatory network. Thus, levels of cis-regulatory divergence or drift appear to be governed by distinct structural constraints that will be difficult to predict based on network architectur

Genetic Connectivity and Phylogeography of the Branching Vase Sponge (Callyspongia vaginalis) Across Florida and the Caribbean

Chapter 1 The only coral reef ecosystem in the continental USA occurs off southeastern Florida and is under considerable strain due to intense urbanization and coastal development in this region. Coherent management and conservation efforts for this rapidly degrading ecosystem will benefit from knowledge about the patterns of genetic connectivity along the entire Florida reef tract. Because of their substantial biomass and extensive species diversity, the Porifera are an important model for investigating connectivity among coral reefs in Florida. We determined the genetic population structure of a common brooding species, the branching vase sponge, Callyspongia vaginalis, along 465 km of the Florida reef system from Palm Beach to the Dry Tortugas based on sequence data from the mitochondrial cytochrome oxidase subunit 1 (COI) gene. Populations of C. vaginalis were highly structured (overall ΦST=0.33), in some cases over distances as small as tens of kilometers. However, nonsignificant pairwise ΦST values were also found between a few relatively distant sampling sites suggesting that some long distance dispersal, perhaps by means of larval transport via sponge fragments, may occur along continuous, shallow coastlines. Indeed, sufficient gene flow appears to occur along the Florida reef tract to obscure a signal of isolation by distance, but not to homogenize COI haplotype frequencies. There was strong genetic differentiation among most of the sampling locations highlighting the fact that recruitment in this species is largely locally source-driven and that management needs to occur on a local scale. The C. vaginalis population at the northern end of the Florida reef tract (Palm Beach) had the lowest genetic diversity observed. This portion of the reef tract generally receives much less management attention than the southern reefs of the Florida Keys National Marine Sanctuary, and may require targeted conservation efforts for biodiversity preservation. Chapter 2 The Porifera constitute a substantial part of the biomass on coral reefs, frequently have higher species diversity than corals and algae, and promote species richness through the fauna they support, making this phylum an important model for investigating connectivity among coral reefs. However, sponges have been neglected in population level genetic studies, particularly in the Caribbean. We determined genetic connectivity among populations of the branching vase sponge (Callyspongia vaginalis) by analyzing DNA sequence variation in 511bp of the mitochondrial cytochrome oxidase (COI) gene from 401 sponges sampled at 14 locations in Florida and the Caribbean. A significant signal of isolation by distance (P \u3c 0.0001) was detected and an analysis of molecular variance (AMOVA) showed a pattern of high genetic structure among populations (ΦST = 0.57, P \u3c 0.0001) with 82 of 91 pairwise comparisons being significant. Statistical parsimony analysis revealed two highly divergent haplotypes, suggestive of cryptic speciation. Inferences from a nested clade analysis suggested a northward movement out of the hypothesized ancestral population in Central America and into the Gulf of Mexico and Florida. The strong genetic structure observed Caribbean-wide indicates that there is little gene flow among populations and that recruitment of C. vaginalis is driven largely from local sources. As a result, recovery of this species on degraded reefs by seeding from distant, healthier reefs is unlikely. These results underscore the need for reef management and conservation efforts on small spatial scales