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 proposed that reduced seasonal temperature variation selects for narrower thermal tolerances and limited dispersal along tropical elevation gradients [Janzen DH (1967) Am Nat 101:233-249]. These locally adapted traits should, in turn, promote reproductive isolation and higher speciation rates in tropical mountains compared with 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 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.

Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis).

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. 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 Channel Island. Analysis of 5293 SNP loci generated using Restriction-site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations 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.

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.

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 favourable 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 analysed 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 postsettlement 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.

Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata.

There is an ongoing debate on the scale of pelagic larval dispersal in promoting connectivity among populations of shallow, benthic marine organisms. The linearly arranged Hawaiian Islands are uniquely suited to study scales of population connectivity and have been used extensively as a natural laboratory in terrestrial systems. Here, we focus on Hawaiian populations of the lobe coral Porites lobata, an ecosystem engineer of shallow reefs throughout the Pacific. Patterns of recent gene flow and population structure in P. lobata samples (n = 318) from two regions, the Hawaiian Islands (n = 10 sites) and from their nearest neighbour Johnston Atoll, were analysed with nine microsatellite loci. Despite its massive growth form, ∼ 6% of the samples from both regions were the product of asexual reproduction via fragmentation. Cluster analysis and measures of genetic differentiation indicated that P. lobata from the Hawaiian Islands are strongly isolated from those on Johnston Atoll (F(ST) = 0.311; P < 0.001), with the descendants of recent migrants (n = 6) being clearly identifiable. Within the Hawaiian Islands, P. lobata conforms to a pattern of isolation by distance. Here, over 37% (P = 0.001) of the variation in genetic distance was explained by geographical distance. This pattern indicates that while the majority of ongoing gene flow in Hawaiian P. lobata occurs among geographically proximate reefs, inter-island distances are insufficient to generate strong population structure across the archipelago.

Genome-wide patterns of nucleotide polymorphism in domesticated rice.

Domesticated Asian rice (Oryza sativa) is one of the oldest domesticated crop species in the world, having fed more people than any other plant in human history. We report the patterns of DNA sequence variation in rice and its wild ancestor, O. rufipogon, across 111 randomly chosen gene fragments, and use these to infer the evolutionary dynamics that led to the origins of rice. There is a genome-wide excess of high-frequency derived single nucleotide polymorphisms (SNPs) in O. sativa varieties, a pattern that has not been reported for other crop species. We developed several alternative models to explain contemporary patterns of polymorphisms in rice, including a (i) selectively neutral population bottleneck model, (ii) bottleneck plus migration model, (iii) multiple selective sweeps model, and (iv) bottleneck plus selective sweeps model. We find that a simple bottleneck model, which has been the dominant demographic model for domesticated species, cannot explain the derived nucleotide polymorphism site frequency spectrum in rice. Instead, a bottleneck model that incorporates selective sweeps, or a more complex demographic model that includes subdivision and gene flow, are more plausible explanations for patterns of variation in domesticated rice varieties. If selective sweeps are indeed the explanation for the observed nucleotide data of domesticated rice, it suggests that strong selection can leave its imprint on genome-wide polymorphism patterns, contrary to expectations that selection results only in a local signature of variation.

The extent of linkage disequilibrium in rice (Oryza sativa L.).

Despite its status as one of the world's major crops, linkage disequilibrium (LD) patterns have not been systematically characterized across the genome of Asian rice (Oryza sativa). Such information is critical to fully exploit the genome sequence for mapping complex traits using association techniques. Here we characterize LD in five 500-kb regions of the rice genome in three major cultivated rice varieties (indica, tropical japonica, and temperate japonica) and in the wild ancestor of Asian rice, Oryza rufipogon. Using unlinked SNPs to determine the amount of background linkage disequilibrium in each population, we find that the extent of LD is greatest in temperate japonica (probably >500 kb), followed by tropical japonica (approximately 150 kb) and indica (approximately 75 kb). LD extends over a shorter distance in O. rufipogon (<<40 kb) than in any of the O. sativa groups assayed here. The differences in the extent of LD among these groups are consistent with differences in outcrossing and recombination rate estimates. As well as heterogeneity between groups, our results suggest variation in LD patterns among genomic regions. We demonstrate the feasibility of genomewide association mapping in cultivated Asian rice using a modest number of SNPs.

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.

BACKGROUND: 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. METHODOLOGY/PRINCIPAL FINDINGS: 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. CONCLUSIONS/SIGNIFICANCE: 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.