skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Genetic adaptation despite high gene flow in a range‐expanding population
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.  more » « less
Award ID(s):
1924537 1924505 1924604
PAR ID:
10582142
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ;
Publisher / Repository:
Molecular Ecology
Date Published:
Journal Name:
Molecular Ecology
ISSN:
0962-1083
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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. 
    more » « less
  2. Abstract Anthropogenic changes have altered the historical distributions of many North American taxa. As environments shift, ecological and evolutionary processes can combine in complex ways to either stimulate or inhibit range expansion. Here, we examined the role of evolution in a rapid range expansion whose ecological context has been well‐documented, Anna's Hummingbird (Calypte anna). Previous studies have suggested that theC. annarange expansion is the result of an ecological release facilitated by human‐mediated environmental changes, where access to new food sources have allowed further filling of the abiotic niche. We examined the role of gene flow and adaptation during range expansion from their native California breeding range, north into Canada and east into New Mexico and Texas, USA. Using low coverage whole genome sequencing we found high genetic diversity, low divergence, and little evidence of selection on the northern and eastern expansion fronts. Additionally, there are no clear barriers to gene flow across the native and expanded range. The lack of selective signals between core and expanded ranges could reflect (i) an absence of novel selection pressure in the expanded range (supporting the ecological release hypothesis), (ii) swamping of adaptive variation due to high gene flow, or (iii) limitations of genome scans for detecting small shifts in allele frequencies across many loci. Nevertheless, our results provide an example where strong selection is not apparent during a rapid, contemporary range shift. 
    more » « less
  3. Marine species worldwide are responding to ocean warming by shifting their ranges to new latitudes and, for intertidal species, elevations. Demographic traits can vary across populations spanning latitudinal and elevational ranges, with impacts on population growth. Understanding how demography varies across gradients from range center to edge could help us predict future shifts, species assemblages, and extinction risks. We investigated demographic traits for 2 range-expanding whelk species:Acanthinucella spirataandMexacanthina lugubris.We measured reproductive output across environmental (latitudinal and shore elevation) gradients along the coast of California, USA. We also conducted intensive measurements of offspring condition (survival and thermal tolerance) across shore elevation forM. lugubrisat one site. We found no difference in reproductive output, body size, or larval survival across shore heights forM. lugubris,suggesting that egg-laying behavior buffers developing stages from the relatively high level of thermal variation experienced due to daily tidal emersion. However, across latitudes, reproductive output increased toward the leading range edge forA. spirata, and body size increased for both species. Increased vital rates at the leading range edge could increase whelk population growth and expansion, allowing species to persist under climate change even if contractions occur at trailing edges. 
    more » « less
  4. Campbell, Barbara J (Ed.)
    ABSTRACT Photoautotrophic diazotrophs, specifically the generaTrichodesmiumand UCYN-A, play a pivotal role in marine nitrogen cycling through their capacity for nitrogen fixation. Despite their global distribution, the microdiversity and environmental drivers of these diazotrophs remain underexplored. This study provides a comprehensive analysis of the global diversity and distribution ofTrichodesmiumand UCYN-A using the nitrogenase gene (nifH) as a genetic marker. We sequenced 954 samples from the Pacific, Atlantic, and Indian Oceans as part of the Bio-GO-SHIP project. Our results reveal significant phylogenetic and biogeographic differences between and within the two genera.Trichodesmiumexhibited greater microdiversity compared to UCYN-A, with clades showing region-specific distribution.Trichodesmiumclades were primarily influenced by temperature and nutrient availability. They were particularly frequent in regions of phosphorus stress. In contrast, UCYN-A was most frequently observed in regions experiencing iron stress. UCYN-A clades demonstrated more homogeneous distributions, with a single sequence variant within the UCYN-A1 clade dominating across varied environments. The biogeographic patterns and environmental correlations ofTrichodesmiumand UCYN-A highlight the role of microdiversity in their ecological adaptation and reflect their different ecological strategies. These findings underscore the importance of characterizing the global patterns of fine-scale genetic diversity to better understand the functional roles and distribution of marine nitrogen-fixing photoautotrophs.IMPORTANCEThis study provides insights into the global diversity and distribution of nitrogen-fixing photoautotrophs, specificallyTrichodesmiumand UCYN-A. We sequenced 954 oceanic samples of thenifHnitrogenase gene and uncovered significant differences in microdiversity and environmental associations between these genera.Trichodesmiumshowed high levels of sequence diversity and region-specific clades influenced by temperature and nutrient availability. In contrast, UCYN-A exhibited a more uniform distribution, thriving in iron-stressed regions. Quantifying these fine-scale genetic variations enhances our knowledge of their ecological roles and adaptations, emphasizing the need to characterize the genetic diversity of marine nitrogen-fixing prokaryotes. 
    more » « less
  5. 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 these 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. 
    more » « less