Mass mortalities in natural populations, particularly those that leave few survivors over large spatial areas, may cause long-term ecological perturbations. Yet mass mortalities may remain ...undocumented or poorly described due to challenges in responding rapidly to unforeseen events, scarcity of baseline data, and difficulties in quantifying rare or patchily distributed species, especially in remote or marine systems. Better chronicling the geographic pattern and intensity of mass mortalities is especially critical in the face of global changes predicted to alter regional disturbance regimes. Here, we couple replicated post-mortality surveys with preceding long-term surveys and historical data to describe a rapid and severe mass mortality of rocky shore invertebrates along the north-central California coast of the northeastern Pacific Ocean. In late August 2011, formerly abundant intertidal populations of the purple sea urchin (Strongylocentrotus purpuratus, a well-known ecosystem engineer), and the predatory six-armed sea star (Leptasterias sp.) were functionally extirpated from ~100 km of coastline. Other invertebrates, including the gumboot chiton (Cryptochiton stelleri) the ochre sea star (Pisaster ochraceus), and subtidal populations of purple sea urchins also exhibited elevated mortality. The pattern and extent of mortality suggest the potential for long-term population, community, and ecosystem consequences, recovery from which may depend on the different dispersal abilities of the affected species.
Aim
Theory predicts that differences in phylogeographic structure between species should be related to differences in life history, environment, and evolutionary time. Reviews of empirical studies ...suggest sometimes complex interactions and possibly a preponderance of exceptions to the predicted relationship that greater population genetic differentiation results from lower dispersal potential, as a function of life history. We apply an analytical framework, which controls for effects of environment and time, to test the hypothesis that contrasts in population genetic differentiation are proportional to contrasts in life history traits.
Location
Global.
Methods
We conducted a meta‐analysis using contrasts of life history traits and population genetic differentiation between synchronously diverging codistributed (SDC) taxa. Because SDC taxa experienced the same environment at the same time, the effects of time and environment are effectively controlled when analysing other causes of genetic differentiation within SDC taxa. This offers the opportunity to rigorously test whether traits favouring greater dispersal potential—such as fecundity, census population size, and duration of the dispersive stage—do lead to lower population genetic differentiation.
Results
We find a strong inverse relationship between dispersal potential and population genetic differentiation, consistent with predictions. SDC species pairs with similar dispersal potential show similar population genetic differentiation; species with higher dispersal potential have lower population genetic differentiation, relative to species with lower dispersal potential.
Main conclusions
SDC comparisons provide a rigorous method for disentangling the factors driving patterns of genetic differentiation in the marine and nonmarine realms. We found broad support for the relationship that higher dispersal potential is associated with lower population genetic differentiation, the specifics of which can be influenced by place, time, and taxon. This relationship appears to be stronger on land than in the sea. However, many factors influence population genetic structure; deviations in measured versus predicted population genetic differentiation may indicate the influence of drift or selection. Too often, too many factors go unmeasured, constraining our ability to disaggregate dispersal syndromes and fully resolve the influence of specific life history characteristics on gene flow.
Standing genetic variation enables or restricts a population’s capacity to respond to changing conditions, including the extreme disturbances expected to increase in frequency and intensity with ...continuing anthropogenic climate change. However, we know little about how populations might respond to extreme events with rapid genetic shifts, or how population dynamics may influence and be influenced by population genomic change. We use a range-wide epizootic, sea star wasting disease, that onset in mid-2013 and caused mass mortality in Pisaster ochraceus to explore how a keystone marine species responded to an extreme perturbation. We integrated field surveys with restriction site-associated DNA sequencing data to (i) describe the population dynamics of mortality and recovery, and (ii) compare allele frequencies in mature P. ochraceus before the disease outbreak with allele frequencies in adults and new juveniles after the outbreak, to identify whether selection may have occurred. We found P. ochraceus suffered 81% mortality in the study region between 2012 and 2015, and experienced a concurrent 74-fold increase in recruitment beginning in late 2013. Comparison of pre- and postoutbreak adults revealed significant allele frequency changes at three loci, which showed consistent changes across the large majority of locations. Allele frequency shifts in juvenile P. ochraceus (spawned from premortality adults) were consistent with those seen in adult survivors. Such parallel shifts suggest detectable signals of selection and highlight the potential for persistence of this change in subsequent generations, which may influence the resilience of this keystone species to future outbreaks.
The extent of parallel genomic responses to similar selective pressures depends on a complex array of environmental, demographic, and evolutionary forces. Laboratory experiments with replicated ...selective pressures yield mixed outcomes under controlled conditions and our understanding of genomic parallelism in the wild is limited to a few well‐established systems. Here, we examine genomic signals of selection in the eelgrass Zostera marina across temperature gradients in adjacent embayments. Although we find many genomic regions with signals of selection within each bay there is very little overlap in signals of selection at the SNP level, despite most polymorphisms being shared across bays. We do find overlap at the gene level, potentially suggesting multiple mutational pathways to the same phenotype. Using polygenic models we find that some sets of candidate SNPs are able to predict temperature across both bays, suggesting that small but parallel shifts in allele frequencies may be missed by independent genome scans. Together, these results highlight the continuous rather than binary nature of parallel evolution in polygenic traits and the complexity of evolutionary predictability.
Theoretically, species' characteristics should allow estimation of dispersal potential and, in turn, explain levels of population genetic differentiation. However, a mismatch between traits and ...genetic patterns is often reported for marine species, and interpreted as evidence that life‐history traits do not influence dispersal. Here, we couple ecological and genomic methods to test the hypothesis that species with attributes favouring greater dispersal potential—e.g., longer pelagic duration, higher fecundity and larger population size—have greater realized dispersal overall. We used a natural experiment created by a large‐scale and multispecies mortality event which created a “clean slate” on which to study recruitment dynamics, thus simplifying a usually complex problem. We surveyed four species of differing dispersal potential to quantify the abundance and distribution of recruits and to genetically assign these recruits to probable parental sources. Species with higher dispersal potential recolonized a broader extent of the impacted range, did so more quickly and recovered more genetic diversity than species with lower dispersal potential. Moreover, populations of taxa with higher dispersal potential exhibited more immigration (71%–92% of recruits) than taxa with lower dispersal potential (17%–44% of recruits). By linking ecological with genomic perspectives, we demonstrate that a suite of interacting life‐history and demographic attributes do influence species' realized dispersal and genetic neighbourhoods. To better understand species' resilience and recovery in this time of global change, integrative eco‐evolutionary approaches are needed to more rigorously evaluate the effect of dispersal‐linked attributes on realized dispersal and population genetic differentiation.
The inclusion of next‐generation sequencing technologies in population genetic and phylogenetic studies has elevated the need to balance time and cost of DNA extraction without compromising DNA ...quality. We tested eight extraction methods – ranging from low‐ to high‐throughput techniques – and eight phyla: Annelida, Arthropoda, Cnidaria, Chordata, Echinodermata, Mollusca, Ochrophyta and Porifera. We assessed DNA yield, purity, efficacy and cost of each method. Extraction efficacy was quantified using the proportion of successful polymerase chain reaction (PCR) amplification of two molecular markers for metazoans (mitochondrial COI and nuclear histone 3) and one for Ochrophyta (mitochondrial nad6) at four time points – 0.5, 1, 2 and 3 years following extraction. DNA yield and purity were quantified using NanoDrop absorbance ratios. Cost was estimated in terms of time and material expense. Results show differences in DNA yield, purity and PCR success between extraction methods and that performance also varied by taxon. The traditional time‐intensive, low‐throughput CTAB phenol–chloroform extraction performed well across taxa, but other methods also performed well and provide the opportunity to reduce time spent at the bench and increase throughput.
Aim
We consider the opportunities and challenges comparative phylogeography (CP) faces in the genomic age to determine: (1) how we can maximise the potential of big CP analyses to advance ...biogeographic and macroevolutionary theory; and (2) what we can, and will struggle, to achieve using CP approaches in this era of genomics.
Location
World‐wide.
Taxon
All.
Methods
We review the literature to discuss the future of CP ‐ particularly examining CP insights enabled by genomics that may not be possible for single species and/or few molecular markers. We focus on how geography and species' natural histories interact to yield congruent and incongruent patterns of neutral and adaptive processes in the context of both historical and recent rapid evolution. We also consider how CP genomic data are being stored, accessed, and shared.
Results
With the widespread availability of genomic data, the shift from a single‐ to a multi‐locus perspective is resulting in detailed historical inferences and an improved statistical rigour in phylogeography. However, the time and effort required for collecting co‐distributed species and accruing species‐specific ecological knowledge continue to be limiting factors. Bioinformatic skills and user‐friendly analytical tools, alongside the computational infrastructure required for big data, can also be limiting.
Main conclusions
Over the last ~35 years, there has been much progress in understanding how intraspecific genetic variation is geographically distributed. The next major steps in CP will be to incorporate evolutionary processes and community perspectives to account for patterns and responses among co‐distributed species and across temporal scales, including those related to anthropogenic change. However, the full potential of CP will only be realised if we employ robust study designs within a sound comparative framework. We advocate that phylogeographers adopt such consistent approaches to enhance future comparisons to present‐day findings.
Abstract
Wildlife diseases, such as the sea star wasting (SSW) epizootic that outbroke in the mid-2010s, appear to be associated with acute and/or chronic abiotic environmental change; dissociating ...the effects of different drivers can be difficult. The sunflower sea star, Pycnopodia helianthoides, was the species most severely impacted during the SSW outbreak, which overlapped with periods of anomalous atmospheric and oceanographic conditions, and there is not yet a consensus on the cause(s). Genomic data may reveal underlying molecular signatures that implicate a subset of factors and, thus, clarify past events while also setting the scene for effective restoration efforts. To advance this goal, we used Pacific Biosciences HiFi long sequencing reads and Dovetail Omni-C proximity reads to generate a highly contiguous genome assembly that was then annotated using RNA-seq-informed gene prediction. The genome assembly is 484 Mb long, with contig N50 of 1.9 Mb, scaffold N50 of 21.8 Mb, BUSCO completeness score of 96.1%, and 22 major scaffolds consistent with prior evidence that sea star genomes comprise 22 autosomes. These statistics generally fall between those of other recently assembled chromosome-scale assemblies for two species in the distantly related asteroid genus Pisaster. These novel genomic resources for P. helianthoides will underwrite population genomic, comparative genomic, and phylogenomic analyses—as well as their integration across scales—of SSW and environmental stressors.
Documenting ecological patterns across spatially, temporally and taxonomically diverse ecological communities is necessary for a general understanding of the processes shaping biodiversity. A major ...gap in our understanding remains the comparison of diversity patterns across a broad spectrum of evolutionarily and functionally diverse organisms, particularly in the marine realm. Here, we aim to narrow this gap by comparing the diversity patterns of free-living microbes and macro-invertebrates across a natural experiment provided by the marine lakes of Palau: geographically discrete and environmentally heterogeneous bodies of seawater with comparable geological and climatic history, and a similar regional species pool. We find contrasting patterns of α-diversity but remarkably similar patterns of β-diversity between microbial and macro-invertebrate communities among lakes. Pairwise dissimilarities in community composition among lakes are positively correlated between microbes and macro-invertebrates, and influenced to a similar degree by marked gradients in oxygen concentration and salinity. Our findings indicate that a shared spatio-temporal and environmental context may result in parallel patterns of β-diversity in microbes and macro-invertebrates, in spite of key trait differences between these organisms. This raises the possibility that parallel processes also influence transitions among regional biota across the tree of life, at least in the marine realm.
Beginning in 2013, sea stars throughout the Eastern North Pacific were decimated by wasting disease, also known as “asteroid idiopathic wasting syndrome” (AIWS) due to its elusive aetiology. The ...geographic extent and taxonomic scale of AIWS meant events leading up to the outbreak were heterogeneous, multifaceted, and oftentimes unobserved; progression from morbidity to death was rapid, leaving few tell‐tale symptoms. Here, we take a forensic genomic approach to discover candidate genes that may help explain sea star wasting syndrome. We report the first genome and annotation for Pisaster ochraceus, along with differential gene expression (DGE) analyses in four size classes, three tissue types, and in symptomatic and asymptomatic individuals. We integrate nucleotide polymorphisms associated with survivors of the wasting disease outbreak, DGE associated with temperature treatments in P. ochraceus, and DGE associated with wasting in another asteroid Pycnopodia helianthoides. In P. ochraceus, we found DGE across all tissues, among size classes, and between asymptomatic and symptomatic individuals; the strongest wasting‐associated DGE signal was in pyloric caecum. We also found previously identified outlier loci co‐occur with differentially expressed genes. In cross‐species comparisons of symptomatic and asymptomatic individuals, consistent responses distinguish genes associated with invertebrate innate immunity and chemical defence, consistent with context‐dependent stress responses, defensive apoptosis, and tissue degradation. Our analyses thus highlight genomic constituents that may link suspected environmental drivers (elevated temperature) with intrinsic differences among individuals (age/size, alleles associated with susceptibility) that elicit organismal responses (e.g., coelomocyte proliferation) and manifest as sea star wasting mass mortality.
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