Decline of melanism in two British moths: spatial, temporal and inter-specific variation

Cook, L. M.; Turner, John R. G.

doi:10.1038/hdy.2008.105

Cited by 51 publications

(20 citation statements)

References 41 publications

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“…The fitness cost estimate was approximately 0.2 (CI: 0.19-0.215) if assumed constant, and could be reduced in the ENE only by accepting an implausibly large increase at the opposite end of the cline. The magnitude of our estimate is consistent with estimates obtained using a different method (29) from records of continuous change at seven United Kingdom sites (including three on our transect). Previous models constructed to account for the spatial variation in carbonaria frequencies have assumed a value for adult male migration of 2.5 km/day (10, 13), liberally derived from one MRR experiment (9), and that effects of gene flow in different directions tend to cancel out (29,30).…”

Section: Independent Estimates Of Dispersalsupporting

confidence: 79%

Selection and gene flow on a diminishing cline of melanic peppered moths

Saccheri

Rousset

Watts

et al. 2008

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

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Historical datasets documenting changes to gene frequency clines are extremely rare but provide a powerful means of assessing the strength and relative roles of natural selection and gene flow. In 19th century Britain, blackening of the environment by the coalfired manufacturing industry gave rise to a steep cline in the frequency of the black (carbonaria) morph of the peppered moth (Biston betularia) across northwest England and north Wales. The carbonaria morph has declined across the region following 1960s legislation to improve air quality, but the cline had not been comprehensively described since the early 1970s. We have quantified changes to the cline as of 2002, equivalent to an interval of 30 generations, and find that a cline still exists but that it is much shallower and shifted eastward. Joint estimation of the dominant fitness cost of carbonaria and dispersal parameters consistent with the observed cline change indicate that selection against carbonaria is very strong across the landscape (s Ϸ 0.2), and that dispersal is much greater than previously assumed. The high dispersal estimate is further supported by the weak pattern of genetic isolation by distance at microsatellite loci, and it implies that in addition to adult dispersal, wind-dispersed first instar larvae also contribute to lifetime dispersal. The historical perspective afforded by this study of cline reversal provides new insight into the factors contributing to gene frequency change in this species, and it serves to illustrate that, even under conditions of high dispersal and strong reverse selection acting against it, complete erosion of an established cline requires many generations.Biston betularia ͉ industrial melanism ͉ cline change S ystematic changes in phenotype or genotype along an environmental gradient, or clines, are among the most visible signals of ongoing or recent selection in nature. If, through a change in environmental conditions, the selection producing the cline ceases to operate, gene flow, brought about by dispersal, will homogenize the differences, eventually eliminating the cline. The time required for this process can be predicted (1), but to do so it is necessary to evaluate the interacting effects of selection, gene flow, effective population size, and mutation. Industrial melanism in the peppered moth, Biston betularia, represents a textbook example of a pulse of gene frequency change that gave rise to a cline, followed by reduction in frequency after the selection reversed in direction. The purpose of this study is to quantify changes to the cline in northwest England and Wales during the latter phase spanning 30 years, and to evaluate the roles of selection and gene flow in producing this change.The cline of melanic B. betularia arose in the second half of the 19th century, following the appearance of a completely black morph (known as carbonaria) first recorded from Manchester, in northwest England, in 1848, although a museum specimen of unknown provenance dates from before 1811 (2). A large body of evid...

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Section: Independent Estimates Of Dispersalsupporting

confidence: 79%

Selection and gene flow on a diminishing cline of melanic peppered moths

Saccheri

Rousset

Watts

et al. 2008

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

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“…Reviews of measurements of selection in nature have emphasized the scarcity of such continuous, longterm studies, especially of invertebrates, despite their value in determining the intensity and the variability of selection under natural conditions (Hendry and Kinnison, 1999;Hoekstra et al, 2001;Hereford et al, 2004;Siepielski et al, 2009). The classic example of directional selection on industrial melanism in the moth Biston betularia (for example, Cook and Turner, 2008) and the analysis of fluctuating selection on shell banding in T. pisana over 34 years at Bold Park (Johnson, 2011a) provide the most thorough temporal studies of selection in polymorphic invertebrates in natural populations.…”

Section: Introductionmentioning

confidence: 99%

Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana

Johnson

2011

Heredity

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Hotter conditions favour effectively unbanded (EUB) shells in the snail Theba pisana. T. pisana is also polymorphic for colour of the shell's apex, determined by a pair of alleles at a locus linked to the banding locus. Apex colour is epistatic to shell banding, such that banded snails with a dark apex have darker bands. Annual censuses over 22 years across an ecotone between a sheltered Acacia thicket and open dune vegetation showed a persistent association of both EUB shells and pale apex with the Open habitat. The parallel variation was due partly to strong phenotypic disequilibrium, as the combination of EUB with dark apex was rare. Nevertheless, in fully banded shells the frequency of pale apex was also higher in the Open habitat, confirming independent, parallel associations of the two contributors to paleness. Within the Acacia habitat, temporal variation of the frequencies of banding morphs was much greater than for apex colour, and EUB shells were associated with hotter summers. Consistent with its primary effect only on the very small snails, apex colour did not vary with summer conditions, but instead, higher frequencies of pale apices were associated with sunnier winters. The intensity of selection was lower on apex colour than shell banding, due partly to the constraint of phenotypic disequilibrium. The shell traits in T. pisana are an example of complex responses to climatic variation, in which phenotypic disequilibrium constrains evolution of apex colour, but separate mechanisms of selection are evident.

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“…Those authors also highlighted two other limitations in the temporal studies of natural selection: (1) studies are heavily biased towards vertebrates (for example, their 11 longest studies were all of vertebrates, representing only 8 genera); and (2) it is easier to detect selection than to understand causes, and relatively few temporal studies (see, for example, Grant and Grant, 2002;McAdam and Boutin, 2003;Carlson and Quinn, 2007) test clear adaptive hypotheses. An exception to both limitations is the analysis of industrial melanism in the moth Biston betularia (for example, Cook and Turner, 2008), but additional, focused studies of invertebrates are clearly needed.…”

Section: Introductionmentioning

confidence: 99%

Thirty-four years of climatic selection in the land snail Theba pisana

Johnson

2010

Heredity

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Few continuous, long-term studies have measured the intensity and variability of natural selection within a framework of clear adaptive hypotheses. In the snail Theba pisana, the proportion of effectively unbanded shells is higher in exposed habitats than in adjacent acacia thickets, which has been explained by microclimatic selection. Comparisons across an ecotone for 34 consecutive years determined the combined effects on morph frequencies of habitat and changes in weather conditions during summer. The long-term average ( ± s.e.) frequency of effectively unbanded shells was 0.577 ± 0.011 in the open habitat when compared with 0.353±0.005 in the acacia. The persistent association of shell banding with habitat accounted for 34% of the variation in morph frequencies. Differences among years were also large, representing 23% of the variation. Higher proportions of effectively unbanded snails were associated with hotter, sunnier summers. Thus, temporal variation supports the hypothesis of microclimatic selection, consistent with the spatial association with habitat. Based on observed rates of change, the mean annual selection on this polymorphism was about 0.13, but with a large variance: s was as high as 0.5, but p0.05 in about 40% of the years. The large variance and frequent reversals in direction of selection indicate a potential for rapid genetic change, but with little net change in morph frequencies over three decades, highlighting the value of long-term continuous studies of populations facing natural environmental variation.

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Decline of melanism in two British moths: spatial, temporal and inter-specific variation

Cited by 51 publications

References 41 publications

Selection and gene flow on a diminishing cline of melanic peppered moths

Selection and gene flow on a diminishing cline of melanic peppered moths

Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana

Thirty-four years of climatic selection in the land snail Theba pisana

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