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ABSTRACT How reproductive barriers arise in early stages of divergence among broadcast spawning organisms that exist in sympatry remains poorly understood. Reproductively isolated lineages (Clade A and B) ofStichopuscf.horrenswere previously reported across the western Pacific, with an additional putative cryptic species detected within the Clade B lineage warranting further examination. The present study further examines the hypothesis that the two mitochondrial lineages (Clade A and Clade B) ofStichopuscf. horrensrepresent putative cryptic species and whether another cryptic species within the Clade B lineage exists using a reduced representation genomic approach. Using double‐digest RAD (ddRAD) sequencing, a total of 9788 single nucleotide polymorphism (SNP) markers were used to examine divergence amongStichopuscf. horrenslineages (n = 82). Individuals grouped into three SNP genotype clusters, broadly concordant with their mitochondrial lineages and microsatellite genotype clusters, with limited gene flow inferred among clusters. Outlier analysis recovered highly divergent SNP loci with significant homology to proteins related to rhodopsin and tachykinin receptor signaling, sperm motility, transmembrane transport, and hormone response. This study confirms the existence of three reproductively isolated genotype clusters withinStichopuscf.horrensand highlights gene regions related to reproduction that may contribute to establishing reproductive barriers between broadcast spawning species at an early stage of divergence. 

ABSTRACT Microbiomes have gained significant attention in ecological research, owing to their diverse interactions and essential roles within different organismal ecosystems. Microorganisms, such as bacteria, archaea, and viruses, have profound impact on host health, influencing digestion, metabolism, immune function, tissue development, and behavior. This study investigates the microbiome diversity and function of Kellet’s whelk (Kelletia kelletii) perivitelline fluid (PVF), which sustains thousands of developingK. kelletiiembryos within a polysaccharide and protein matrix. Our core microbiome analysis reveals a diverse range of bacteria, with theRoseobactergenus being the most abundant. Additionally, genes related to host-microbe interactions, symbiosis, and quorum sensing were detected, indicating a potential symbiotic relationship between the microbiome and Kellet’s whelk embryos. Furthermore, the microbiome exhibits gene expression related to antibiotic biosynthesis, suggesting a defensive role against pathogenic bacteria and potential discovery of novel antibiotics. Overall, this study sheds light on the microbiome’s role in Kellet’s whelk development, emphasizing the significance of host-microbe interactions in vulnerable life history stages. To our knowledge, ours is the first study to use 16S sequencing coupled with RNA sequencing (RNA-seq) to profile the microbiome of an invertebrate PVF.IMPORTANCEThis study provides novel insight to an encapsulated system with strong evidence of symbiosis between the microbial inhabitants and developing host embryos. The Kellet’s whelk perivitelline fluid (PVF) contains microbial organisms of interest that may be providing symbiotic functions and potential antimicrobial properties during this vulnerable life history stage. This study, the first to utilize a comprehensive approach to investigating Kellet’s whelk PVF microbiome, couples 16S rRNA gene long-read sequencing with RNA-seq. This research contributes to and expands our knowledge on the roles of beneficial host-associated microbes. 

Abstract Signals of natural selection can be quickly eroded in high gene flow systems, curtailing efforts to understand how and when genetic adaptation occurs in the ocean. This long‐standing, unresolved topic in ecology and evolution has renewed importance because changing environmental conditions are driving range expansions that may necessitate rapid evolutionary responses. One example occurs in Kellet's whelk (Kelletia kelletii), a common subtidal gastropod with an ~40‐ to 60‐day pelagic larval duration that expanded their biogeographic range northwards in the 1970s by over 300 km. To test for genetic adaptation, we performed a series of experimental crosses with Kellet's whelk adults collected from their historical (HxH) and recently expanded range (ExE), and conducted RNA‐Seq on offspring that we reared in a common garden environment. We identified 2770 differentially expressed genes (DEGs) between 54 offspring samples with either only historical range (HxH offspring) or expanded range (ExE offspring) ancestry. Using SNPs called directly from the DEGs, we assigned samples of known origin back to their range of origin with unprecedented accuracy for a marine species (92.6% and 94.5% for HxH and ExE offspring, respectively). The SNP with the highest predictive importance occurred on triosephosphate isomerase (TPI), an essential metabolic enzyme involved in cold stress response.TPIwas significantly upregulated and contained a non‐synonymous mutation in the expanded range. Our findings pave the way for accurately identifying patterns of dispersal, gene flow and population connectivity in the ocean by demonstrating that experimental transcriptomics can reveal mechanisms for how marine organisms respond to changing environmental conditions. 

Abstract Scleractinian corals are the main modern builders of coral reefs, which are major hot spots of marine biodiversity. Southern Atlantic reef corals are understudied compared to their Caribbean and Indo‐Pacific counterparts and many hypotheses about their population dynamics demand further testing. We employed thousands of single nucleotide polymorphisms (SNPs) recovered via ezRAD to characterize genetic population structuring and species boundaries in the amphi‐Atlantic hard coral genusFavia. Coalescent‐based species delimitation (BFD* – Bayes Factor Delimitation) recoveredF. fragumandF. gravidaas separate species. Although our results agree with depth‐related genetic structuring inF. fragum, they did not support incipient speciation of the ‘tall’ and ‘short’ morphotypes. The preferred scenario also revealed a split between two main lineages ofF. gravida, one from Ascension Island and the other from Brazil. The Brazilian lineage is further divided into a species that occurs throughout the Northeastern coast and another that ranges from the Abrolhos Archipelago to the state of Espírito Santo. BFD* scenarios were corroborated by analyses of SNP matrices with varying levels of missing data and by a speciation‐based delimitation approach (DELINEATE). Our results challenge current notions about Atlantic reef corals because they uncovered surprising genetic diversity inFaviaand rejected the long‐standing hypothesis that Abrolhos Archipelago may have served as a Pleistocenic refuge during the last glaciations. 

Abstract Introduced and invasive species make excellent natural experiments for investigating rapid evolution. Here, we describe the effects of genetic drift and rapid genetic adaptation in pink salmon (Oncorhynchus gorbuscha) that were accidentally introduced to the Great Lakes via a single introduction event 31 generations ago. Using whole‐genome resequencing for 134 fish spanning five sample groups across the native and introduced range, we estimate that the source population's effective population size was 146,886 at the time of introduction, whereas the founding population's effective population size was just 72—a 2040‐fold decrease. As expected with a severe founder event, we show reductions in genome‐wide measures of genetic diversity, specifically a 37.7% reduction in the number of SNPs and an 8.2% reduction in observed heterozygosity. Despite this decline in genetic diversity, we provide evidence for putative selection at 47 loci across multiple chromosomes in the introduced populations, including missense variants in genes associated with circadian rhythm, immunological response and maturation, which match expected or known phenotypic changes in the Great Lakes. For one of these genes, we use a species‐specific agent‐based model to rule out genetic drift and conclude our results support a strong response to selection occurring in a period gene (per2) that plays a predominant role in determining an organism's daily clock, matching large day length differences experienced by introduced salmon during important phenological periods. Together, these results inform how populations might evolve rapidly to new environments, even with a small pool of standing genetic variation. 

Abstract From genes to communities, understanding how diversity is maintained remains a fundamental question in biology. One challenging to identify, yet potentially ubiquitous, mechanism for the maintenance of diversity is negative frequency dependent selection (NFDS), which occurs when entities (e.g., genotypes, life history strategies, species) experience a per capita reduction in fitness with increases in relative abundance. Because NFDS allows rare entities to increase in frequency while preventing abundant entities from excluding others, we posit that negative frequency dependent selection plays a central role in the maintenance of diversity. In this review, we relate NFDS to coexistence, identify mechanisms of NFDS (e.g., mutualism, predation, parasitism), review strategies for identifying NFDS, and distinguish NFDS from other mechanisms of coexistence (e.g., storage effects, fluctuating selection). We also emphasize that NFDS is a key place where ecology and evolution intersect. Specifically, there are many examples of frequency dependent processes in ecology, but fewer cases that link this process to selection. Similarly, there are many examples of selection in evolution, but fewer cases that link changes in trait values to negative frequency dependence. Bridging these two well‐developed fields of ecology and evolution will allow for mechanistic insights into the maintenance of diversity at multiple levels. 

Abstract How to identify the drivers of population connectivity remains a fundamental question in ecology and evolution. Answering this question can be challenging in aquatic environments where dynamic lake and ocean currents coupled with high levels of dispersal and gene flow can decrease the utility of modern population genetic tools. To address this challenge, we used RAD‐Seq to genotype 959 yellow perch (Perca flavescens), a species with an ~40‐day pelagic larval duration (PLD), collected from 20 sites circumscribing Lake Michigan. We also developed a novel, integrative approach that couples detailed biophysical models with eco‐genetic agent‐based models to generate “predictive” values of genetic differentiation. By comparing predictive and empirical values of genetic differentiation, we estimated the relative contributions for known drivers of population connectivity (e.g., currents, behavior, PLD). For the main basin populations (i.e., the largest contiguous portion of the lake), we found that high gene flow led to low overall levels of genetic differentiation among populations (F_ST = 0.003). By far the best predictors of genetic differentiation were connectivity matrices that were derived from periods of time when there were strong and highly dispersive currents. Thus, these highly dispersive currents are driving the patterns of population connectivity in the main basin. We also found that populations from the northern and southern main basin are slightly divergent from one another, while those from Green Bay and the main basin are highly divergent (F_ST = 0.11). By integrating biophysical and eco‐genetic models with genome‐wide data, we illustrate that the drivers of population connectivity can be identified in high gene flow systems. 

Understanding connectivity between populations is key to identifying hotspots of diversity, dispersal sinks and sources, and effective management units for natural resources. Multi-species connectivity seeks to overcome species-specific idiosyncrasies to identify shared patterns that are most critical to spatial management. The linear Hawaiian archipelago provides an excellent platform to assess multi-species connectivity patterns, with shared boundaries to gene flow identified across a majority of the 41 coral reef species surveyed to date. Here, we evaluate genome-scale data by comparing consistency and resolution to previous connectivity studies using far fewer loci. We used pool-seq to genotype 22,503–232,730 single nucleotide polymorphisms per species (625,215 SNPs total) from the same individuals published in previous studies of two fishes, two corals, and two lobsters. Additionally, one coral species (Pocillopora meandrina) without previous archipelago-wide population genetic data was included. With greater statistical power, most genetic differences between pairwise comparisons of islands were significant (250 of 308), consistent with the most recent larval dispersal models for the Hawaiian Archipelago. These data reveal significant differentiation at a finer scale than previously reported using single-marker studies, yet did not overturn any of the conclusions or management implications drawn from previous studies. We confirm that population genomic datasets are consistent with previously reported patterns of multispecies connectivity but add a finer layer of population resolution that is pertinent to management. 

Silky shark (Carcharhinus falciformis,Carcharhinidae) numbers have declined steeply in recent decades due to the fin fishery and bycatch in pelagic fisheries. Due to a lack of data on stock delineations, this species is currently managed in ocean-spanning jurisdictions defined by regional fisheries management organizations (RFMOs). Here we investigate the global stock structure of silky sharks and compare population structure to the four RFMO boundaries. Using high-throughput sequencing from pooled individuals (pool-seq) based on 628 specimens collected opportunistically across 11 circumglobal regions, yielding 854 nuclear single nucleotide polymorphisms (SNPs) and 23 mtDNA SNPs. Results indicate significant population genetic structure between all 11 regional sampling locations, with discriminant analysis of principal components (DAPC) identifying seven discrete groups. Within the Atlantic and Indo-Pacific Oceans,F_STvalues ranged from 0.014 to 0.035 for nuclear (nDNA) markers, and from 0.012 to 0.160 for whole mtDNA genomes, with much higher values between than within oceans (mtDNA: 0.383–0.844, nDNA: 0.042–0.078). Using an analysis of molecular variance (AMOVA) framework, 22.24% of the observed population variance is explained by RFMOs, 32.1% is explained among ocean basins, and 34.81% is explained by the DAPC-identified groups. We find significant population genetic structure within the jurisdiction of every RFMO, from which we have more than a single sampling site. Our genomic-scale results indicate discordance between population genetic structure and RFMOs, highlighting the need for a detailed study to accurately identify stock boundaries. 

Climate-driven warming and changes in major ocean currents enable poleward larval transport and range expansions of many marine species. Here, we report the population genetic structure of the gastropodKelletia kelletii, a commercial fisheries species and subtidal predator with top-down food web effects, whose populations have recently undergone climate-driven northward range expansion. We used reduced representation genomic sequencing (RAD-seq) to genotype 598 adults from 13 locations spanning approximately 800 km across the historical and expanded range of this species. Analyses of 40747 single nucleotide polymorphisms (SNPs) showed evidence for long-distance dispersal ofK. kelletiilarvae from a central historical range site (Point Loma, CA, USA) hundreds of km into the expanded northern range (Big Creek, CA), which seems most likely to result from transport during an El Niño-Southern Oscillation (ENSO) event rather than consistent on-going gene flow. Furthermore, the high genetic differentiation among some sampled expanded-range populations and their close genetic proximity with distinct populations from the historical range suggested multiple origins of the expanded-range populations. Given that the frequency and magnitude of ENSO events are predicted to increase with climate change, understanding the factors driving changes in population connectivity is crucial for establishing effective management strategies to ensure the persistence of this and other economically and ecologically important species.