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Wares, J. P.

Publications and source records attributed to Wares, J. P..

10 recordsLinked to original sources

Ocean current models predict spatial structure for coastal biodiversity

Genomic diversity provides the raw material through which all evolutionary processes occur. Accurately describing how environmental features affect patterns of diversity shows promise in predicting the resilience of populations and entire communities to dynamic environments and novel stressors. Identifying the contribution of purely neutral responses to environmental effects can be difficult, especially across large spatial ranges with many covarying environmental features. Using an individual-based model of larvae carried by ocean currents, we predict patterns of neutral genomic diversity in a passively dispersed coastal species, suggesting large geographic regions of relative homogeneity with ancestry determined by the nearest "upstream" population with limited larval input. The genomic identity that dominates each region sharply transitions at the next such interruption, generating hierarchical structure and violating assumptions of isolation-by-distance. We call these upstream populations "lineage source regions" (LSRs), and we find strong concordance between LSR model predictions and an empirical population genomic survey of a keystone salt marsh mussel (Geukensia demissa). We quantitatively validate model performance and goodness-of-fit, updating baseline predictions of genomic diversity patterns from the classic isolation-by-distance model to this LSR framework. This spatially explicit coastal ancestry model has potential for generalization across passive dispersing species.

evolutionary biology↗

The genome of the Pacific acorn barnacle provides insights into the evolution of extremely large populations

Population size is a key factor underlying the mode and tempo of evolution, particularly as it relates to the strength of selection and drift. While the mechanisms underlying the interactions between population size and selection have been studied in population genetics for over a century, empirical knowledge of these dynamics has been limited to species with small-to-moderate historical population sizes. This gap in knowledge highlights the need for empirical studies in systems with historically large population sizes and elevated diversity. The Pacific acorn barnacle (Balanus glandula) presents an exceptional model to study evolution in extremely large populations, exhibiting census sizes often exceeding the tens of thousands of individuals per square meter. We generated a new chromosome-level genome assembly for this species, which we leverage in one of the first large-scale genomic analyses in this system. This assembly reveals a highly polymorphic genome with over 3% heterozygosity. At a population level, B. glandula exhibits extreme levels of polymorphism, with nucleotide diversity surpassing 5% genome-wide in just a small collection of individuals. Across the genome, nucleotide diversity predictably decreases at functional elements, including both coding and non-coding sequences, likely reflecting strong purifying selection along the genome. At the same time, McDonald-Kreitman tests reveal that the majority of non-synonymous substitutions between barnacle species were driven by positive selection, consistent with the expected increase in the efficacy of selection in large populations. These remarkable levels of diversity set B. glandula as a unique model for the study of evolution at extreme demographic scales and highlights the importance of testing evolutionary theory across a wide variety of empirical systems.

evolutionary biology↗

Genomic separation of Salish Sea and Pacific outer coast populations of the keystone sea star Pisaster ochraceus

Understanding dispersal and population structure in marine species is critical to forecasting ecological responses to climate change. The ochre sea star (Pisaster ochraceus), an intertidal keystone predator along the North American Pacific coast, has long been considered to have little spatial genetic structure due to its extended larval dispersal period and thus high potential for gene flow. Here we characterize the spatial genomic architecture of P. ochraceus using whole-genome sequencing (WGS) data from individuals spanning over 3,000km of coastline from Alaska to southern California. Our analyses of putatively neutral SNPs evince considerable mixing throughout the latitudinal range yet reveal substantial population structure between outer Pacific coast populations and those residing within the semi-enclosed estuary of the Salish Sea, suggesting restricted gene flow and demographic divergence between these regions. Genomic divergence is further supported by evidence of selection, with outlier loci highlighting extended regions of low diversity in the Salish Sea, consistent with recent selective sweeps and potential local adaptation to the distinct estuarine conditions. These findings are consistent with the role of oceanographic barriers or environmental heterogeneity in shaping population structure in P. ochraceus, challenging an earlier notion of range-wide homogeneity. By exploring neutral and adaptive genetic diversity in this keystone marine species, we provide valuable insights for its capacity to persist in a rapidly changing world.

evolutionary biology↗

Genomic variation in amylase in Geukensia demissa may be environmentally driven

Prior results suggested an unusual sequence polymorphism in an amylase gene region of the ribbed mussel Geukensia demissa. We used targeted sequencing, spatial analysis of polymorphism data and a high-quality de novo genome assembly to assess the likelihood that this diversity is inherited as a single Mendelian locus. Our results suggest this is likely, and that the frequencies of the dominant allele groups change dramatically along the Atlantic coast of the United States, particularly across Cape Hatteras. The single-copy nature of the sequence being studied was verified through the development of a new reference genome for Geukensia demissa, described here. Although the overall pattern of sequence diversity is atypical, with much higher allelic divergence than is expected given overall genomic diversity, we believe this may be an ecologically valuable molecular marker for study in ribbed mussels.

evolutionary biology↗

Drivers of genetic diversity across the marine tree of life

Why do some species have more genetic diversity than others? This question is one of the greatest remaining mysteries in evolutionary biology, yet we still know little about what factors predict genetic diversity among species. Efforts to quantify diversity or understand its distribution have been hampered by a lack of genomic data analyzed in a consistent way with statistical approaches that can move beyond the population level to generate species-wide estimates of genetic diversity. We address this critical gap by generating standardized estimates of genomic-level genetic diversity for 93 species sampled over 9,000 localities. Because marine species have evolved a strikingly diverse array of biological traits that have long been hypothesized to affect species-level genetic diversity, we focus our study on marine taxa. For each species, we aggregated biotic traits related to life history and abiotic features of the species range. We show that genetic diversity increases with species range extent and planktonic dispersal. We hypothesize that these traits increase a species ability to avoid or recover from bottlenecks, thereby maintaining genetic diversity. Our findings provide insights into how biotic and abiotic factors interact to shape genomic variation in the ocean, and offer a predictive framework for understanding marine biodiversity in the face of global change. Significance statementSpecies exhibit vast trait diversity that allows populations to persist. However, diversity in these traits -- e.g., how organisms reproduce, disperse, and feed -- is not easily linked to what is known of genomic diversity, even in well-studied organisms. We investigate a diverse assemblage of marine species to begin to build a predictive framework for how species traits drive genomic diversity across the worlds oceans. We find that species with larger geographic ranges have higher genomic diversity. More dispersive species also harbor higher diversity, suggesting that greater dispersal facilitates resilience to environmental change. As available datasets increase, our ability to understand fundamental links between trait and genetic diversity and how they shape species responses to environmental change will continue to improve.

evolutionary biology↗

The role of pigments in light color variation of the firefly Photinus pyralis

Fireflies use bioluminescent signals to communicate with their mates. Luciferase has been thought to be the sole contributor to light color; however, populations of the Photinus pyralis firefly display variation in the color of their emitted signals yet have identical luciferase sequences. Here, we examined whether pigments could be present in the light organs of the twilight-active species P. pyralis and contribute to this variation. We detected patterns of expression that suggest ommochrome and pterin screening pigments are expressed in P. pyralis light organs and could filter light emitted by luciferase and play a role in signal tuning. There were no significant differences between the pigment gene expression of P. pyralis individuals with yellower and greener signals. Our study provides alternative mechanisms that could influence pigments in P. pyralis light organs that could also play a role in modifying signal color.

evolutionary biology↗

Mitochondrial diversity in the ribbed mussel, Geukensia demissa, relative to high marsh plant diversity at the southern edge of the distribution

Genomic diversity and relatedness among sample sites are often used to explore landscape-level processes of how and where organisms are limited in movement. In many cases, these patterns of diversity and relatedness can be useful for understanding larger ecological patterns. A prior study has suggested that larval input - inferred from landscape genomic data - of the ribbed mussel Geukensia demissa, a species with important roles in stabilizing salt marsh ecosystems, could be indicative of longer-term recruitment patterns of high marsh plant species. Here we use new observations of mitochondrial diversity in the same region but with more sites sampled to show that this prior study was wrong in suggesting that relationship. The same mitochondrial data are useful for monitoring cryptic patterns of climate response in these mussels relative to a subtropical congener.

ecology↗

Comparative phylogeography of the freshwater mussels of the southeastern United States: reconstructing historic drainages using molecular data

Knowledge of species ages and their distribution enhance our understanding of processes that create and maintain species diversity at both local and regional levels. The largest family of freshwater mussels (Unionidae), reach their highest species diversity in drainages of the southeastern united states. By sequencing multiple loci from mussel species distributed throughout the drainages in this region, we attempt to uncover historical patterns of divergence and determine the role of vicariance events on the species formation in mussels and extend our hypothesis to freshwater animals in general. We analyzed 346 sequences from five genera encompassing 37 species. Species were sampled across 12 distinct drainages ending either in the Atlantic Ocean or the Gulf of Mexico. Overall the topologies of the different genera returned phylogenetic trees that were congruent with geographically contiguous drainages. The most common pattern was the grouping between the Atlantic slope and gulf coast drainages, however the Tennessee drainage was often the exception to this pattern grouping with the Atlantic slope. Most mussel species find a most recent common ancestor within a drainage before finding an ancestor between drainages. This supports the hypothesis of allopatric divergence followed by later burst of speciation within a drainage. Our estimated divergence times for the Atlantic-Gulf split agree with other studies estimating vicariance in fish species of the Atlantic and gulf coast.

evolutionary biology↗

Evidence for boundary layer oxygen diffusion limitation as a key driver of asteroid wasting

Sea star wasting disease describes a condition affecting asteroids that resulted in significant Northeastern Pacific population decline following a mass mortality event in 2013. The etiology of sea star wasting is unresolved. We hypothesized that asteroid wasting is a sequela of microbial organic matter remineralization near respiratory surfaces which leads to boundary layer oxygen diffusion limitation (BLODL). Wasting lesions were induced in Pisaster ochraceus by enrichment with a variety of organic matter (OM) sources and by experimentally reduced oxygen conditions. Microbial assemblages inhabiting tissues and at the asteroid-water interface bore signatures of copiotroph proliferation before wasting onset, followed by the proliferation of putatively facultative and strictly anaerobic taxa. These results together illustrate that suboxic conditions at the animal-water interface may be established by heterotrophic bacterial activity in response to organic matter loading. Wasting susceptibility was significantly and positively correlated with rugosity, a key determinant of boundary layer thickness. At a semi-continuously monitored field site (Langley Harbor), wasting predictably occurred at annual peak or decline in phytoplankton biomass over 5 years, suggesting that primary production-derived OM may contribute to BLODL. Finally, wasting individuals from 2013 - 2014 bore stable isotopic signatures reflecting anaerobic processes which suggests that this phenomenon may have affected asteroids during mass mortality. The impacts of BLODL may be more pronounced under higher temperatures due to lower O2 solubility, in more rugose asteroid species due to restricted hydrodynamic flow, and in larger specimens due to their lower surface area to volume ratios which affects diffusive respiratory potential. Moreover, our results demonstrate that marine invertebrate disease may result from heterotrophic microbial activity that occurs adjacent to respiratory tissues, which raises important questions about the etiology of marine diseases in other benthic taxa.

ecology↗

Re-evaluation of homozygous lethality for EF1A indel polymorphism in Pisaster ochraceus

A genotypic polymorphism in the sea star Pisaster ochraceus has been associated with possible overdominant maintenance of diversity, and subsequent studies of this polymorphism suggested that intermittent disease outbreaks could be a driving factor in this system. However, comparative transcriptomic studies of individuals carrying distinct genotypes at the elongation factor 1-alpha (EF1A) region indicated that the marker was not accurately describing the constitutive differences among individuals. Here we more thoroughly assess this EF1A intron region to better understand how polymorphic diversity could be associated with differential disease outcomes and physiological responses, and find that the underlying genetic model is incorrect. In fact, rather than an instance of homozygous lethality, it is clear that previous genotyping efforts were misled by a PCR artefact. We reanalyze results from two previous studies to show that the effects are not as clear as believed.

evolutionary biology↗