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Nemoralis Shell Polymorphism in the Pyrenees Over Five Decades

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Nemoralis Shell Polymorphism in the Pyrenees Over Five Decades 1 Qualitative and quantitative methods show stability in patterns of Cepaea 2 nemoralis shell polymorphism in the Pyrenees over five decades 3 Daniel Ramos-Gonzalez*1 and Angus Davison2 4 School of Life Sciences, University Park, University of Nottingham, NG7 2RD, UK. 5 1. Email: [email protected], https://orcid.org/0000-0003-4497-6374 6 2. Email: [email protected], https://orcid.org/0000-0003-2554-8585 1 7 Abstract 8 One of the emerging strengths of working with the land snail genus Cepaea is that historical 9 collections can be compared against modern day samples, for instance to understand the 10 impact of changing climate and habitat upon shell morph frequencies. However, one 11 potential limitation is that prior studies scored shell ground colour by eye, usually in the field, 12 into three discrete colours yellow, pink or brown. This incurs both potential error and bias in 13 comparative surveys. In this study, we therefore aimed to use a quantitative method to score 14 shell colour, and evaluated it by comparing patterns of C. nemoralis shell colour 15 polymorphism, using both methods on present day samples, and against historical data 16 gathered in the 1960s using the traditional method. The Central Pyrenees were used as an 17 exemplar, because previous intensive surveys sometimes showed sharp discontinuities of 18 morph frequencies within and between valleys. Moreover, selective factors, such as climate 19 or the human impact in the Pyrenees, have significantly changed since 1960s. The main 20 finding was that while quantitative measures of shell colour reduced the possibility of error, 21 and standardised the procedure, the same altitudinal trends were recovered, irrespective of 22 the method. There was remarkable stability in the local shell patterns over five decades, with 23 the exception of one valley that has been subject to increased human activity. Therefore, 24 although subject to potential error, human-scoring of snail colour data remains valuable, 25 especially if persons have appropriate training. In comparison, while there are benefits in 26 taking quantitative measures of colour in the laboratory, there are also several practical 27 disadvantages, mainly in terms of throughput and accessibility. In the future, we anticipate 28 that both methods may be combined, for example, using automated measures of colour 29 taken from photos generated by citizen scientists conducting field surveys. 2 30 Introduction 31 Historically, two of the most important species in studying colour polymorphism have been 32 the west European land snails Cepaea nemoralis and C. hortensis, because individuals are 33 relatively easy to collect and study, and the colour and banding morphs show straightforward 34 inheritance (Cain & Sheppard, 1950, Cain & Sheppard, 1952, Cain & Sheppard, 1954, 35 Lamotte, 1959, Jones et al., 1977). In the present day, one of the continuing benefits of 36 working with Cepaea is an ability to compare the frequencies of shell morphs in historic 37 collections against modern day samples, to infer the potential impact of natural selection 38 and/or drift in changing shell morph frequencies. Of particular use, the “Evolution Megalab” 39 project digitised a large set of 20th century samples (Silvertown et al., 2011, Cameron & 40 Cook, 2012, Worthington et al., 2012). These records, and others deposited in museums, 41 are now being used with modern surveys to produce an increasing number of comparative 42 papers (Cowie & Jones, 1998, Silvertown et al., 2011, Cameron & Cook, 2012, Ożgo & 43 Schilthuizen, 2012, Worthington et al., 2012, Cameron et al., 2013, Cook, 2014). 44 In nearly all comparative studies of Cepaea reported to date, absolute change in 45 frequencies of the main shell morphs, colour and banding, have been reported, but the 46 direction is not always consistent. The conclusions are in part dependent upon the 47 geographic scale and the precision of resampling, whether exact or nearest neighbour. To 48 fully understand changes − or stasis − in shell polymorphism, both global and local surveys 49 are needed (Berjano et al., 2015). For instance, large-scale surveys illustrate the broad 50 picture of the changes in the spatial variation of the polymorphism. In the largest study, a 51 historical dataset of more than six thousand population samples of C. nemoralis was 52 compared with new data on nearly three thousand populations (Silvertown et al., 2011). A 53 historic geographic cline among habitats in the frequency of the yellow shells was shown to 54 have persisted into the present day. However, there was also an unexpected decrease in 55 the frequency of unbanded shells, and a corresponding increase in frequency of banded 56 and mid-banded morph particularly (Silvertown et al., 2011). A UK-wide study also used 57 Evolution Megalab data, but reported a somewhat different pattern of change. Yellow and 58 mid-banded morphs had increased in woodland, whereas unbanded and mid-banded 59 increased in hedgerow habitats (Cook, 2014). 60 In comparison to these large surveys, the majority of comparative studies have been 61 at a more local scale. The benefit of these is that resampling is often precise (Cowie & Jones, 62 1998, Cook et al., 1999, Ożgo & Schilthuizen, 2012, Cameron et al., 2013, Ożgo et al., 63 2017), and it is also possible to take local factors into account. Most of the original historic 64 studies took place in the UK. Following resampling, modern comparative surveys have 65 tended to find an increase in yellow and mid-banded shells (as above) (Silvertown et al., 66 2011, Ożgo & Schilthuizen, 2012, Cameron et al., 2013, Ożgo et al., 2017), but with 67 exceptions (Cowie & Jones, 1998, Cook et al., 1999, Cameron & Cook, 2012), depending 68 upon the precise scale of comparison. Moreover, patterns of change are not always 69 consistent within the same study. 70 One potential limitation of all of these works is that shell ground colour was scored 71 by eye, usually in the field, into three discrete colours yellow, pink or brown. Even if persons 72 are trained, there is still bias and error, and potential for dispute over what defines each 73 colour. In practise, it is frequently difficult to distinguish the colours, and define different 74 shades of the same colour. Therefore, to understand whether colour variation is in reality 75 continuous, and to investigate how the variation may be perceived by an avian predator, 76 psychophysical models of colour vision were applied to shell reflectance measures, finding 77 that both achromatic and chromatic variation are continuously distributed over many 78 perceptual units in indiscrete in Cepaea nemoralis (Davison et al., 2019). Nonetheless, 3 79 clustering analysis based on the density of the distribution did reveal three groups, roughly 80 corresponding to human-perceived yellow, pink and brown shells. 81 This prior work raises the possibility that reproducible, quantitative shell colour 82 measures, based on spectrophotometry in the laboratory, can be used to compare and test 83 regular shell colour data, avoiding the requirement to bin measures into colour categories. 84 In this study, we therefore aimed 1) to use the quantitative method to score shell colour, and 85 2) evaluated it by comparing patterns of C. nemoralis shell colour polymorphism using both 86 methods on present day samples, and against historical data gathered using the traditional 87 method. 88 To achieve this aim, the Central Pyrenees were used as an exemplar location, 89 because they were intensively surveyed during the 1960s and 70s (Figure 1), sometimes 90 showing sharp discontinuities of frequencies of morphs (Arnold, 1968, Arnold, 1969, 91 Cameron et al., 1973, Jones & Irving, 1975) and genotypes (Ochman et al., 1983) within 92 and between. They are also particularly interesting for their geographic and ecological 93 variation, including a diverse range of different microclimates, within and among the valleys, 94 due to the interaction of three main climates, Atlantic, Mediterranean and Alpine, as well as 95 a large altitudinal differences and incidence of precipitation. Moreover, selective factors, 96 such as climate or the human impact in the Pyrenees, have significantly changed since the 97 1960s (García-Ruiz, 2015). 98 The main finding was that while quantitative measures of shell colour reduced the 99 possibility of error, and standardised the procedure, the same altitudinal trends were 100 recovered, irrespective of the method. There was remarkable a stability in the local shell 101 patterns over five decades. Overall, while there are key benefits in taking quantitative 102 measures of colour in the laboratory, there are also several practical disadvantages. In the 103 future, with the increasing use of digital cameras to capture and record species presence, 104 there is the potential that colour and banding data may be extracted from the images 105 uploaded to public databases and apps such as iRecord, iNaturalist and SnailSnap (Harvey, 106 2018, Horn et al., 2018, Kerstes et al., 2019). For the moment, the fact remains that human- 107 scoring of snail colour data is valuable, especially with appropriate training. 4 108 Materials and Methods 109 Shell samples and human-scoring of shell phenotype 110 The Valle de Vielha, Valle de Jueu, Valle Noguera de Tort and Valle Noguera Ribagorzana, 111 hereafter abbreviated as “Vielha”, “Jueu”, “Tort” and “Riba”, were selected for sampling 112 (Figure 1). This is because they had been previously sampled in 1962 by Arnold (1968), and 113 in 1966 and 1969 by Cameron et al. (1973), with the colour and banding data made available 114 via the Evolution Megalab database. New samples were collected in October 2017 and June 115 2018. By choice, we aimed to sample in the same location as described in past surveys, 116 using the coordinates recorded in the Megalab database; when this was not possible, 117 samples were collected from the nearest adjacent site with suitable habitat for snails.
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