skip to main content

Title: Two distinct population clusters of northern sand lance ( Ammodytes dubius ) on the northwest Atlantic shelf revealed by whole genome sequencing

Northern sand lance (Ammodytes dubius) are essential forage fish in most offshore, temperate-to-polar waters on the Northwest Atlantic shelf (NWA), but their population structure and genetic separation from the American sand lance (A. americanus) remain unresolved. We assembled a reference genome for A. dubius (first in the Ammodytidae) and then used low-coverage whole genome sequencing on 262 specimens collected across the species distribution (Mid-Atlantic Bight to Greenland) to quantify genetic differentiation between geographic regions based on single nucleotide polymorphisms. We found strong separation between A. dubius from locations north and south of the Scotian Shelf, largely due to massive genetic differentiation spanning most of chromosomes 21 and 24. Genetic distance increased with geographic distance in the smaller southern cluster but not in the larger northern cluster, where genetic homogeneity appeared across large geographic distances (>103 km). The two genetic clusters coincide with a clear break in winter sea surface temperature, suggesting that differential offspring survival, rather than limited transport, causes a break in realized connectivity. Nuclear and mitochondrial DNA both clearly delineated A. dubius from A. americanus, thereby confirming a species boundary through spatial niche partitioning into inshore (A. americanus) and offshore (A. dubius) sand lance species on the NWA.

; ; ; ; ; ; ; ; ; ; ; ;
Award ID(s):
Publication Date:
Journal Name:
ICES Journal of Marine Science
Page Range or eLocation-ID:
p. 122-132
Oxford University Press
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Spatial models show that genetic differentiation between populations can be explained by factors ranging from geographic distance to environmental resistance across the landscape. However, genomes exhibit a landscape of differentiation, indicating that multiple processes may mediate divergence in different portions of the genome. We tested this idea by comparing alternative geographic predctors of differentiation in ten bird species that co-occur in Sonoran and Chihuahuan Deserts of North America. Using population-level genomic data, we described the genomic landscapes across species and modeled conditions that represented historical and contemporary mechanisms. The characteristics of genomic landscapes differed across species, influenced by varying levels of population structuring and admixture between deserts, and the best-fit models contrasted between the whole genome and partitions along the genome. Both historical and contemporary mechanisms were important in explaining genetic distance, but particularly past and current environments, suggesting that genomic evolution was modulated by climate and habitat There were also different best-ftit models across genomic partitions of the data, indicating that these regions capture different evolutionary histories. These results show that the genomic landscape of differentiation can be associated with alternative geographic factors operating on different portions of the genome, which reflect how heterogeneous patterns of genetic differentiationmore »can evolve across species and genomes.

    « less
  2. Abstract

    The study of local adaptation in the presence of ongoing gene flow is the study of natural selection in action, revealing the functional genetic diversity most relevant to contemporary pressures. In addition to individual genes, genome-wide architecture can itself evolve to enable adaptation. Distributed across a steep thermal gradient along the east coast of North America, Atlantic silversides (Menidia menidia) exhibit an extraordinary degree of local adaptation in a suite of traits, and the capacity for rapid adaptation from standing genetic variation, but we know little about the patterns of genomic variation across the species range that enable this remarkable adaptability. Here, we use low-coverage, whole-transcriptome sequencing of Atlantic silversides sampled along an environmental cline to show marked signatures of divergent selection across a gradient of neutral differentiation. Atlantic silversides sampled across 1371 km of the southern section of its distribution have very low genome-wide differentiation (median FST = 0.006 across 1.9 million variants), consistent with historical connectivity and observations of recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs) are nearly fixed (FST > 0.95) for alternate alleles. Highly differentiated SNPs cluster into four tight linkage disequilibrium (LD) blocks that span hundreds of genes and several megabases. Variants in thesemore »LD blocks are disproportionately nonsynonymous and concentrated in genes enriched for multiple functions related to known adaptations in silversides, including variation in lipid storage, metabolic rate, and spawning behavior. Elevated levels of absolute divergence and demographic modeling suggest selection maintaining divergence across these blocks under gene flow. These findings represent an extreme case of heterogeneity in levels of differentiation across the genome, and highlight how gene flow shapes genomic architecture in continuous populations. Locally adapted alleles may be common features of populations distributed along environmental gradients, and will likely be key to conserving variation to enable future responses to environmental change.

    « less
  3. Abstract

    The mitonuclear species concept hypothesizes that incompatibilities between interacting gene products of the nuclear and mitochondrial genomes are a major factor establishing and maintaining species boundaries. However, most of the data available to test this concept come from studies of genetic variation in mitochondrial DNA, and clines in the mitochondrial genome across contact zones can be produced by a variety of forces. Here, we show that using a combination of population genomic analyses of the nuclear and mitochondrial genomes and studies of mitochondrial function can provide insight into the relative roles of neutral processes, adaptive evolution, and mitonuclear incompatibility in establishing and maintaining mitochondrial clines, using Atlantic killifish (Fundulus heteroclitus) as a case study. There is strong evidence for a role of secondary contact following the last glaciation in shaping a steep mitochondrial cline across a contact zone between northern and southern subspecies of killifish, but there is also evidence for a role of adaptive evolution in driving differentiation between the subspecies in a variety of traits from the level of the whole organism to the level of mitochondrial function. In addition, studies are beginning to address the potential for mitonuclear incompatibilities in admixed populations. However, population genomic studiesmore »have failed to detect evidence for a strong and pervasive influence of mitonuclear incompatibilities, and we suggest that polygenic selection may be responsible for the complex patterns observed. This case study demonstrates that multiple forces can act together in shaping mitochondrial clines, and illustrates the challenge of disentangling their relative roles.

    « less
  4. Ojaveer, Henn (Ed.)
    Abstract Northern sand lance (Ammodytes dubius) and Atlantic herring (Clupea harengus) represent the dominant lipid-rich forage fish species throughout the Northeast US shelf and are critical prey for numerous top predators. However, unlike Atlantic herring, there is little research on sand lance or information about drivers of their abundance. We use intra-annual measurements of sand lance diet, growth, and condition to explain annual variability in sand lance abundance on the Northeast US Shelf. Our observations indicate that northern sand lance feed, grow, and accumulate lipids in the late winter through summer, predominantly consuming the copepod Calanus finmarchicus. Sand lance then cease feeding, utilize lipids, and begin gonad development in the fall. We show that the abundance of C. finmarchicus influences sand lance parental condition and recruitment. Atlantic herring can mute this effect through intra-guild predation. Hydrography further impacts sand lance abundance as increases in warm slope water decrease overwinter survival of reproductive adults. The predicted changes to these drivers indicate that sand lance will no longer be able to fill the role of lipid-rich forage during times of low Atlantic herring abundance—changing the Northeast US shelf forage fish complex by the end of the century.
  5. Secor, David (Ed.)
    Abstract The Northeast US shelf ecosystem is undergoing unprecedented changes due to long-term warming trends and shifts in regional hydrography leading to changes in community composition. However, it remains uncertain how shelf occupancy by the region's dominant, offshore small pelagic fishes, also known as forage fishes, has changed throughout the late 20th and early 21st centuries. Here, we use species distribution models to estimate the change in shelf occupancy, mean weighted latitude, and mean weighted depth of six forage fishes on the Northeast US shelf, and whether those trends were linked to coincident hydrographic conditions. Our results suggest that observed shelf occupancy is increasing or unchanging for most species in both spring and fall, linked both to gear shifts and increasing bottom temperature and salinity. Exceptions include decreases to observed shelf occupancy by sand lance and decreases to Atlantic herring's inferred habitat suitability in the fall. Our work shows that changes in shelf occupancy and inferred habitat suitability have varying coherence, indicating complex mechanisms behind observed shelf occupancy for many species. Future work and management can use these results to better isolate the aspects of forage fish life histories that are important for determining their occupancy of the Northeast USmore »shelf.« less