Physiological stress and the fitness effects of Mpi genotypes in the acorn barnacle Semibalanus balanoides

Flight, Patrick A.; Schoepfer, Shane D.; Rand, David M.

doi:10.3354/meps08504

Cited by 10 publications

(10 citation statements)

References 39 publications

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“…However, due to the lack of genome information, we are unable to annotate the gene function of these loci. Despite this, our results are consistent with previous studies on invertebrates that intra-population variation in stress tolerance depends on genotype (Watt 1977;Flight et al 2010).…”

Section: Genetic Basis Of Differential Thermal Tolerancesupporting

confidence: 93%

Effects of balancing selection and microhabitat temperature variations on heat tolerance of the intertidal black mussel Septifer virgatus

2020

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Realistic assessments of the impacts of global warming on population extinction risk are likely to require an integrated analysis of the roles of standing genetic variation, microhabitat thermal complexity, and the inter‐individual variation of heat tolerance due to both genetic differences and seasonal acclimatization effects. Here, we examine whether balancing selection and microhabitat temperature heterogeneity can interact to enhance the population persistence to thermal stress for the black mussel Septifer virgatus. We deployed biomimetic data loggers on the shore to measure the microhabitat‐specific thermal variation from June 2014 to April 2016. Thermal tolerance of specimens was indexed by measuring effects of temperature on heart rate. Genotyping of specimens was performed using double digestion restriction association RADSeq (ddRADseq). Our results show that inter‐individual variations in thermal tolerance correlate significantly with genetic differences at some specific gene loci, and that heterozygotes have higher thermal tolerances than homozygotes. The observed seasonal changes in genotype frequency suggest that these loci are under balancing selection. The ability of thermally resistant heterozygotes to survive in sun‐exposed microhabitats acts to balance the loss of homozygotes during summer and enable the persistence of genetic polymorphisms. Population persistence of the mussel is also facilitated by the micro‐scale variation in temperature, which provides refugia from thermal stress. Our results emphasize that inter‐individual variation in thermal tolerance and in microhabitat heterogeneity in temperature are important for the persistence of populations in rocky shore habitats.

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Section: Genetic Basis Of Differential Thermal Tolerancesupporting

confidence: 93%

Effects of balancing selection and microhabitat temperature variations on heat tolerance of the intertidal black mussel Septifer virgatus

2020

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“…This "mosaic" model of thermal stress provides a potential explanation for why Mpi zonation varies from site to site. In addition, our evidence suggests that zonation is a habitatspecific process emerging from the interaction of many ecological variables, as exemplified by the controlled experiments of Flight et al (24), which showed that mortality from thermal stress in barnacles is affected by osmotic stress.…”

Section: Discussionmentioning

confidence: 58%

“…Consequentially, the interaction of high planktonic gene flow, panmictic settlement (specifically for Mpi), and strong microhabitat selection presents an evolutionary problem for Mpi in barnacles: Beneficial alleles within one microhabitat may not become fixed because offspring are likely to settle into environments that drastically differ from their parents. As such, multiple authors have argued for a role of balancing selection as a multiple-niche polymorphism-sensu Levene (22)-as the mechanism for the maintenance of functional genetic variation at Mpi (8,15,23,24). While ecological and physiological evidence lends support to the hypothesis, a full molecular description of the locus is lacking.…”

Section: Significancementioning

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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“…Interestingly, populations south to the Miramichi River have a similar genetic composition to European populations at the Mpi and Gpi loci (Holm & Bourget 1994), an observation which could have filled in a secondary contact scenario. Mpi and Gpi may possibly be directly involved in the barrier (Flight et al. 2010) but irrespectively of the environment (i.e.…”

mentioning

confidence: 99%

The coupling hypothesis: why genome scans may fail to map local adaptation genes

et al. 2011

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Genomic scans of multiple populations often reveal marker loci with greatly increased differentiation between populations. Often this differentiation coincides in space with contrasts in ecological factors, forming a genetic-environment association (GEA). GEAs imply a role for local adaptation, and so it is tempting to conclude that the strongly differentiated markers are themselves under ecologically based divergent selection, or are closely linked to loci under such selection. Here, we highlight an alternative and neglected explanation: intrinsic (i.e. environment-independent) pre-or post-zygotic genetic incompatibilities rather than local adaptation can be responsible for increased differentiation. Intrinsic genetic incompatibilities create endogenous barriers to gene flow, also known as tension zones, whose location can shift over time. However, tension zones have a tendency to become trapped by, and therefore to coincide with, exogenous barriers due to ecological selection. This coupling of endogenous and exogenous barriers can occur easily in spatially subdivided populations, even if the loci involved are unlinked. The result is that local adaptation explains where genetic breaks are positioned, but not necessarily their existence, which can be best explained by endogenous incompatibilities. More precisely, we show that (i) the coupling of endogenous and exogenous barriers can easily occur even when ecological selection is weak; (ii) when environmental heterogeneity is fine-grained, GEAs can emerge at incompatibility loci, but only locally, in places where habitats and gene pools are sufficiently intermingled to maintain linkage disequilibria between genetic incompatibilities, local-adaptation genes and neutral loci. Furthermore, the association between the locally adapted and intrinsically incompatible alleles (i.e. the sign of linkage disequilibrium between endogenous and exogenous loci) is arbitrary and can form in either direction. Reviewing results from the literature, we find that many predictions of our model are supported, including endogenous genetic barriers that coincide with environmental boundaries, local GEA in mosaic hybrid zones, and inverted or modified GEAs at distant locations. We argue that endogenous genetic barriers are often more likely than local adaptation to explain the majority of Fst-outlying loci observed in genome scan approaches -even when these are correlated to environmental variables.

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Physiological stress and the fitness effects of Mpi genotypes in the acorn barnacle Semibalanus balanoides

Cited by 10 publications

References 39 publications

Effects of balancing selection and microhabitat temperature variations on heat tolerance of the intertidal black mussel Septifer virgatus

Effects of balancing selection and microhabitat temperature variations on heat tolerance of the intertidal black mussel Septifer virgatus

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

The coupling hypothesis: why genome scans may fail to map local adaptation genes

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