Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (\u3ci\u3eUrocyon littoralis\u3c/i\u3e)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are pre- dicted to be strong on islands and both could drive population divergence and specia- tion. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Chan- nel Island. Analysis of 5293 SNP loci generated using Restriction-site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mech- anism driving population divergence among island fox populations. In particular, pop- ulations had exceptionally low genetic variation, small Ne (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome-wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high FST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high FST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small Ne in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential

Gene Discovery in the Threatened Elkhorn Coral: 454 Sequencing of the Acropora palmata Transcriptome

BACKGROUND: Cnidarians, including corals and anemones, offer unique insights into metazoan evolution because they harbor genetic similarities with vertebrates beyond that found in model invertebrates and retain genes known only from non-metazoans. Cataloging genes expressed in Acropora palmata, a foundation-species of reefs in the Caribbean and western Atlantic, will advance our understanding of the genetic basis of ecologically important traits in corals and comes at a time when sequencing efforts in other cnidarians allow for multi-species comparisons. RESULTS: A cDNA library from a sample enriched for symbiont free larval tissue was sequenced on the 454 GS-FLX platform. Over 960,000 reads were obtained and assembled into 42,630 contigs. Annotation data was acquired for 57% of the assembled sequences. Analysis of the assembled sequences indicated that 83-100% of all A. palmata transcripts were tagged, and provided a rough estimate of the total number genes expressed in our samples (~18,000-20,000). The coral annotation data contained many of the same molecular components as in the Bilateria, particularly in pathways associated with oxidative stress and DNA damage repair, and provided evidence that homologs of p53, a key player in DNA repair pathways, has experienced selection along the branch separating Cnidaria and Bilateria. Transcriptome wide screens of paralog groups and transition/transversion ratios highlighted genes including: green fluorescent proteins, carbonic anhydrase, and oxidative stress proteins; and functional groups involved in protein and nucleic acid metabolism, and the formation of structural molecules. These results provide a starting point for study of adaptive evolution in corals. CONCLUSIONS: Currently available transcriptome data now make comparative studies of the mechanisms underlying coral's evolutionary success possible. Here we identified candidate genes that enable corals to maintain genomic integrity despite considerable exposure to genotoxic stress over long life spans, and showed conservation of important physiological pathways between corals and bilaterians

Location-Specific Responses to Thermal Stress in Larvae of the Reef-Building Coral Montastraea faveolata

The potential to adapt to a changing climate depends in part upon the standing genetic variation present in wild populations. In corals, the dispersive larval phase is particularly vulnerable to the effects of environmental stress. Larval survival and response to stress during dispersal and settlement will play a key role in the persistence of coral populations.To test the hypothesis that larval transcription profiles reflect location-specific responses to thermal stress, symbiont-free gametes from three to four colonies of the scleractinian coral Montastraea faveolata were collected from Florida and Mexico, fertilized, and raised under mean and elevated (up 1 to 2 degrees C above summer mean) temperatures. These locations have been shown to exchange larvae frequently enough to prevent significant differentiation of neutral loci. Differences among 1,310 unigenes were simultaneously characterized using custom cDNA microarrays, allowing investigation of gene expression patterns among larvae generated from wild populations under stress. Results show both conserved and location-specific variation in key processes including apoptosis, cell structuring, adhesion and development, energy and protein metabolism, and response to stress, in embryos of a reef-building coral.These results provide first insights into location-specific variation in gene expression in the face of gene flow, and support the hypothesis that coral host genomes may house adaptive potential needed to deal with changing environmental conditions

Data from: Narrow thermal tolerance and low dispersal drive higher speciation in tropical mountains

Species richness is greatest in the tropics and much of this diversity is concentrated in mountains. Janzen (1967) proposed that reduced seasonal temperature variation selects for narrower thermal tolerances and limited dispersal along tropical elevation gradients. These locally adapted traits should, in turn, promote reproductive isolation and higher speciation rates in tropical mountains compared to temperate ones. Here we show that tropical and temperate montane stream insects have diverged in thermal tolerance and dispersal capacity, two key traits that are drivers of isolation in montane populations. Tropical species in each of three insect clades have markedly narrower thermal tolerances and lower dispersal than temperate species, resulting in significantly greater population divergence, higher cryptic species diversity, higher tropical speciation rates, and greater accumulation of species over time. Our study also indicates that tropical montane species, with narrower thermal tolerance and reduced dispersal ability, will be especially vulnerable to rapid climate change

Data from: Variation in the transcriptional response of threatened coral larvae to elevated temperatures

Coral populations have declined worldwide largely due to increased sea surface temperatures. Recovery of coral populations depends in part upon larval recruitment. Many corals reproduce during the warmest time of year when further increases in temperature can lead to low fertilization rates of eggs and high larval mortality. Microarray experiments were designed to capture and assess variability in the thermal stress responses of Acropora palmata larvae from Puerto Rico. Transcription profiles showed a striking acceleration of normal developmental gene expression patterns with increased temperature. The transcriptional response to heat suggested rapid depletion of larval energy stores via peroxisomal lipid oxidation and included key enzymes that indicated the activation of the glyoxylate cycle. High temperature also resulted in expression differences in key developmental signalling genes including the conserved WNT pathway that is critical for pattern formation and tissue differentiation in developing embryos. Expression of these and other important developmental and thermal stress genes such as ferritin, heat shock proteins, cytoskeletal components, cell adhesion and autophagy proteins also varied among larvae derived from different parent colonies. Disruption of normal developmental and metabolic processes will have negative impacts on larval survival and dispersal as temperatures rise. However, it appears that variation in larval response to high temperature remains despite the dramatic population declines. Further research is needed to determine whether this variation is heritable or attributable to maternal effects

Data from: No gene flow across the Eastern Pacific Barrier in the reef-building coral Porites lobata

The expanse of deep water between the Central Pacific islands and the continental shelf of the Eastern Tropical Pacific is regarded as the world’s most potent marine biogeographic barrier. During recurrent climatic fluctuations (ENSO - El Niño Southern Oscillation), however, changes in water temperature and the speed and direction of currents become favorable for trans-oceanic dispersal of larvae from central Pacific to marginal Eastern Pacific reefs. Here we investigate the population connectivity of the reef building coral Porites lobata across the Eastern Pacific Barrier (EPB). Patterns of recent gene flow in samples (n=1173) from the Central Pacific and the Eastern Tropical Pacific (ETP), were analyzed with 12 microsatellite loci. Results indicated that P. lobata from the ETP are strongly isolated from those in the central Pacific and Hawaii (F’CT=0.509; P<0.001). However, samples from Clipperton Atoll, an oceanic island on the eastern side of the EPB, grouped with the Central Pacific. Within the Central Pacific, Hawaiian populations were strongly isolated from three co-occurring clusters found throughout the remainder of the Central Pacific. No further substructure was evident in the ETP. Changes in oceanographic conditions during ENSO over the past several thousand years thus appear insufficient to support larval deliveries from the central Pacific to the ETP or strong post-settlement selection acts on ETP settlers from the central Pacific. Recovery of P. lobata populations in the frequently disturbed ETP thus must depend on local larval sources

SuppTableS3_Final

Expression behavior for all probes expressed over background in response to time, temperature, batch, and interactions among the factors. LFC indicates log fold change between treatments. Expression pattern denotes probes that were avove the threshold for significance (LFC>1.5 and Q.value<0.05), and indicates which treatement had higher expression levels

DRYAD_BaumsEtAl_2012_StructureInput

Input file for Structure v 2.3.3. First line contains locus names. One line per individual. Missing data is encoded by -9. Column1: Sample ID; Column2: Population; Column3: Population Flag; Column 4ff: allele size

DRYAD_BaumsEtAl_2012_Plobata_Genotypes

DRYAD_BaumsEtAl_2012_Plobata_Genotype

DRYAD_BaumsEtAl_2012_StructureParameters

Parameters for Structure v 2.3.3