Rare genetic variation and balanced polymorphisms are important for survival in global change conditions

Brennan, Reid S.; Garrett, April D.; Huber, Kaitlin E.; Hargarten, Heidi; Pespeni, Melissa H.

doi:10.1098/rspb.2019.0943

Cited by 48 publications

(61 citation statements)

References 71 publications

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“…Ultimately, these findings contribute to an emerging body of work demonstrating that rapid adaptation can indeed exhibit a polygenic basis 2–4,37 . Variation at functional loci across the genome is likely maintained in populations via multilocus balancing selection between populations spanning environmental gradients 9–12 , or within populations experiencing temporally fluctuating selection pressures 3,38 .…”

Section: Discussionmentioning

confidence: 68%

Standing genetic variation fuels rapid adaptation to ocean acidification

et al. 2019

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Global climate change has intensified the need to assess the capacity for natural populations to adapt to abrupt shifts in the environment. Reductions in seawater pH constitute a conspicuous global change stressor that is affecting marine ecosystems globally. Here, we quantify the phenotypic and genetic modifications associated with rapid adaptation to reduced seawater pH in the Mediterranean mussel, Mytilus galloprovincialis. We reared a genetically diverse larval population in two pH treatments (pHT 8.1 and 7.4) and tracked changes in the shell-size distribution and genetic variation through settlement. Additionally, we identified differences in the signatures of selection on shell growth in each pH environment. Both phenotypic and genetic data show that standing variation can facilitate adaptation to declines in seawater pH. This work provides insight into the processes underpinning rapid evolution, and demonstrates the importance of maintaining variation within natural populations to bolster species’ adaptive capacity as global change progresses.

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Section: Discussionmentioning

confidence: 68%

Standing genetic variation fuels rapid adaptation to ocean acidification

et al. 2019

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“…We tested for zonation using a Cochran-Mantel-Haenszel (CMH) test. CMH is an association test used in population genetics to identify constant and consistent changes in allele frequencies across independent biological replicates (42)(43)(44). For this analysis, we tested for independence between "stress treatment" and allelic ratio "outcome."…”

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confidence: 99%

Footprints of natural selection at the mannose-6-phosphate isomerase locus in barnacles

Nunez

Flight

Neil

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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The mannose-6-phosphate isomerase (Mpi) locus in Semibalanus balanoides has been studied as a candidate gene for balancing selection for more than two decades. Previous work has shown that Mpi allozyme genotypes (fast and slow) have different frequencies across Atlantic intertidal zones due to selection on postsettlement survival (i.e., allele zonation). We present the complete gene sequence of the Mpi locus and quantify nucleotide polymorphism in S. balanoides, as well as divergence to its sister taxon Semibalanus cariosus. We show that the slow allozyme contains a derived charge-altering amino acid polymorphism, and both allozyme classes correspond to two haplogroups with multiple internal haplotypes. The locus shows several footprints of balancing selection around the fast/slow site: an enrichment of positive Tajima’s D for nonsynonymous mutations, an excess of polymorphism, and a spike in the levels of silent polymorphism relative to silent divergence, as well as a site frequency spectrum enriched for midfrequency mutations. We observe other departures from neutrality across the locus in both coding and noncoding regions. These include a nonsynonymous trans-species polymorphism and a recent mutation under selection within the fast haplogroup. The latter suggests ongoing allelic replacement of functionally relevant amino acid variants. Moreover, predicted models of Mpi protein structure provide insight into the functional significance of the putatively selected amino acid polymorphisms. While footprints of selection are widespread across the range of S. balanoides, our data show that intertidal zonation patterns are variable across both spatial and temporal scales. These data provide further evidence for heterogeneous selection on Mpi.

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“…Main Text: Though global conditions are changing at a geologically unprecedented rate and the frequency of extreme events is increasing (11), species can use genetic adaptation or physiological plasticity to persist (12,13). Even over remarkably short time scales, one to four generations, selection can shift populations towards adaptive phenotypes (14)(15)(16)(17)(18)(19). However, we still know little about the genome-wide underpinnings of complex physiological phenotypes, the relative importance of genetic adaptation versus plasticity for responding to environmental changes on different time scales, or the impacts of rapid adaptation on plasticity.…”

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confidence: 99%

“…Genetic adaptation, heritable genetic change that improves the mean fitness of a population in an environment 5 , enables resilience by shifting the mean phenotype of the population to tolerate different conditions. Selection can shift population genetic variation over short time scales, as few as one to four generations, changing population phenotypes to improve mean fitness in response to an extreme change in the environment [6][7][8][9] . Conversely, plasticity allows a single genotype to generate different phenotypes in response to the environment 10 .…”

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confidence: 99%

Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

Brennan

deMayo

Dam

et al. 2020

Preprint

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Global conditions are changing at unprecedented rates (1), challenging species resilience (2). Populations can respond to these changes through genetic adaptation and physiological plasticity (3, 4), and it is well accepted that these processes interact (5). However, the relative role plasticity and adaptation play in promoting resilience to global change and the potential impacts of rapid adaptation on plasticity during this process are not well understood (3, 5–10). Here, using experimental evolution and reciprocal transplantation of the marine coastal copepod, Acartia tonsa, we show rapid adaptation to global change conditions carries costs, notably a loss of physiological plasticity. Twenty generations of selection resulted in rapid, highly parallel adaptation to greenhouse conditions. However, this adaptation reduced plasticity and fitness, particularly when returned to ambient conditions and under food limitation. Due to the loss of plasticity, greenhouse adapted lines could no longer tolerate ambient conditions and compensated by additional adaptive evolution, a process that eroded nucleotide diversity in genes containing adaptive genetic variation for global change conditions. These results show that adaptation can negatively affect plasticity, limiting resilience to new stressors and previously benign environments. Our findings challenge the common assertion that the presence of adaptive genetic potential or physiological plasticity alone will enable population resilience under global change conditions.Significance statementUnderstanding how species will respond to changing environmental conditions is an essential step in mitigating the potential negative consequences of human induced global change conditions. Typically, it is assumed that a species with sufficient plasticity or adaptive potential will be resilient in the face of these changes. Here, we experimentally evolve a copepod to simulated future acidic and warm conditions. We show that rapid adaptation reduced phenotypic plasticity and eroded the adaptive genetic variation necessary to tolerate additional environmental stress. These findings demonstrate that the presence of plasticity or adaptive potential do not necessarily indicate a resilient population, illustrating the importance of considering the interaction between these factors when predicting species tolerance to global change.

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Rare genetic variation and balanced polymorphisms are important for survival in global change conditions

Cited by 48 publications

References 71 publications

Standing genetic variation fuels rapid adaptation to ocean acidification

Standing genetic variation fuels rapid adaptation to ocean acidification

Footprints of natural selection at the mannose-6-phosphate isomerase locus in barnacles

Loss and recovery of transcriptional plasticity after long-term adaptation to global change conditions in a marine copepod

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