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Coelopa Frigida) Heredity 62 (1989) 223-232 The Genetical Society of Great Britain Received 18 July 1988 Environmental correlates of inversion frequencies in natural populations of seaweed flies (Coelopa frigida) R. K. Butlin* and * Departmentof Zoology, University College, T. H. Dayt P.O. Box 78, Cardiff, U.K. t Department of Genetics, Queens Medical Centre, University of Nottingham, Nottingham, U.K. Two populations of seaweed flies (Coelopa frigida) from the north-east coast of England were sampled at approximately monthly intervals. Single samples were also collected from populations on the south coast. The allele and genotype frequencies at the alcohol dehydrogenase locus, known to be associated with the large a/13 chromosomal inversion, were determined for each of the 34 samples. Aspects of the habitats were quantified at the time of sampling, as were 12 variables extracted from meteorological data. The genetic, ecological and climatic data are used to test predictions deriving from laboratory experiments and from previous, smaller scale, sampling programmes. There was an excess of heterokaryotypes over Hardy—Weinberg expectations which was stable over time. While the frequencies were close to the predicted equilibrium values, the rate of return following departures from the equilibrium was more rapid than predicted from the operation of heterokaryotypic advantage alone. Estimates of the effective population size were very much lower than census estimates. Karyotype frequencies cycled seasonally and were associated with both temperature and the incidence of gales. The interactions of ecological and life-historical factors with the observed genetical variation are discussed. INTRODUCTION obscura on which the classical studies of inversion polymorphism were conducted (Wright and Dob- Oneof the principal aims of ecological genetics is zhansky, 1946). to explain the frequencies of genetic variants in The identification of selective agents influenc- natural populations in terms of environmental ing a polymorphism must involve at least two variables. Despite many years of endeavour there phases: correlation of allele or genotype frequen- are still rather few examples for which a clear link cies in natural populations with environmental has been established between specific environ- variables, and manipulation of environmental vari- mental variables and allele frequencies. Among ables in laboratory populations. Only a combina- the best known cases are the visible polymorphisms tion of these two types of observation can establish in Biston betularia (Brakefield, 1987) and Cepaea a link between an environmental variable and the nemoralis (Cain and Shepphard, 1954), allozyme polymorphism, and even then it may be necessary polymorphisms in Mytilus edulis (Koehn, 1978) to demonstrate the mechanistic relationship and Drosophila melanogaster (van Delden, 1982), between the gene and the selective agent to estab- and of course, sickle cell disease in man (Allison, lish that the link is causal (Clarke, 1979). 1954). Even in these species a complete description The habitat of the seaweed fly, Coelopafrigida, of the selection pressures involved is not yet avail- is clearly defined; it lives only in piles of decaying able. Unlike enzyme polymorphisms, there is gen- seaweed cast up on beaches by tides and winds erally no question about the existence of selection (Dobson, 1974a, 1976). So far all populations maintaining chromosomal inversion polymorph- studied in northern Europe are polymorphic for a isms, and the selection pressures may be substan- large inversion on chromosome I (Butlin et a!., tial. Inversion systems should, therefore, be good 1982a; Day et a!., 1983; and unpublished data). candidates for studying the ecological factors Inversion frequencies in natural populations responsible for selection but this approach has not strongly suggest that the polymorphism is been exploited because of the difficulty of defining maintained by selection, and laboratory experi- the natural habitat of species such as D. pseudo- ments indicate that at least three types of selection 224 A. K. BUTLIN AND T. H. DAY may operate: heterokaryotypic advantage in egg (4) depth of seaweed bed (>lm, 02-l0m, to adult viability (Butlin et a!., 1984), variation in <02m, or "strings" among pebbles) development time (Day et a!., 1980), and sexual (5) extent of decomposition (fresh, moderate, selection (Butlin et a!., 1982b, Day et a!., 1987). very decomposed, extremely decomposed, This is therefore a promising system in which to extremely decomposed loose and dry, or study the connection between environmental par- extremely decomposed wet and foul ameters and inversion frequencies. in this paper smelling) we report on a series of samples from natural (6) temperature of seaweed bed relative to air populations and examine the extent to which selec- temperature (cold, cool, warm, hot, or very tion pressures identified in the laboratory can hot) explain variations in the inversion frequencies (7) wetness of seaweed bed (dry, moderate, or observed. wet) (8) size of Coelopa larvae (small, medium, or large) METHODS (9) larval density (sparse, moderate, dense, or very dense) Samplesof seaweed flies were collected as larvae (10) presence or absence of Coelopa adults from ten sites on the north-east and south coasts (11) proportion of Coelopapilipes in the emerging of England from March 1981 to March 1982 (see adults (scored after collection of adults in the Appendix for details of sites). Two sites were laboratory). sampled repeatedly (St. Mary's island, SM, and Meteorological data were obtained from pub- Whitburn, WH) to give a total of 34 samples (12 lished sources (Meteorological Office, Bracknell, from SM, 10 from WH and 12 others). Larvae were Berks.) for Tynemouth, Tyne and Wear (north east kept in the seaweed in which they were collected coast) and Twist, Devon (south coast). The follow- and emerging adults were removed and stored at ing parameters have been considered: —25°C. A sub-sample from the total pool of adults (12) monthly mean temperatures (T) emerging from a collection (often several thousand (13) total monthly rainfall (R) individuals) was used for genetic analysis. (This (14) number of days per month on which a gale is the "larval" method of Butlin et a!., 1982a). was blowing, i.e. wind speed exceeded 34 Chromosome I in C. frigida has two arrange- knots (G) ments, designated a and /3, related by a complex (15) total hours of sunshine per month (S) pattern of overlapping inversions (Aziz, 1975). To Each of these values was cumulated over one, score flies for the inversion we took advantage of two or three months to test for delayed or averaged a close association between the inversion and the effects, giving 12 environmental parameters TI, Adh locus (Day et al., 1982), The Adh-B allele is T2, T3, Ri, R2, R3, Gi, G2, G3 and Si, S2, S3. always found with the a arrangement and the Adh-D allele with the /3. Three other Adh alleles are present; the Adh-C allele which occurs with both arrangements, and the rare Adh-A and -E PREDICTIONS alleles whose inversion associations are unknown. Methods for electrophoresis have been described Thetotal data set consists of 34 samples for each by Butlin et a!., (1982a). For reasons outlined of which the frequencies of six common genotypes below only data on females were used in the analy- and two rare alleles are available, plus up to 23 sis although electrophoresis was carried out on environmental parameters. It is clearly not produc- both sexes. A total of more than 3700 individual tive to test for associations of each genetic par- females were scored from the 34 collections; ameter with each environmental parameter sample sizes are given in the Appendix. because many such tests would give significant In addition to these genetic data, information results due to chance alone. We have, therefore, was also collected at the time of sampling on a made specific predictions about the expected range of environmental variables as follows: associations based on information already avail- (1) date of collection able concerning the a//3 inversion system. This (2) composition of the seaweed bed (mainly places us in a much stronger position when testing Laminaria, Laminaria and Fucus, or mainly for associations in the field data. Fucus) Before describing these predictions it will be (3) area of seaweed bed (large, medium, or small) helpful to consider a caveat about the sampling INVERSION FREQUENCIES IN SEASONAL POPULATIONS 225 procedure. Seaweed beds were sampled at random Prediction 3 times in their life span, which is principally deter- Theviabilities observed in laboratory trials predict mined by the cycle of spring tides and by gales an equilibrium frequency of ainthe region 04-0 5 (Dobson, 1974a). The chromosome I inversion is in the absence of other selection pressures. This known to influence development time (Day eta!., should be reflected in a similar frequency of the 1980)and so there is a very real risk of biased Adh-B allele amongst Adh-B and -D alleles, sampling. We attempted to reduce this bias by although these allele frequencies can vary to some collecting from beds containing only larvae—that extent independently of inversion frequencies is before pupation had started. However, this was because of the presence of the Adh-C allele on not always easy to ascertain and so it is possible both arrangements. that some samples were deficient in the fast Viability selection also predicts that in developing /3f3 karyotype. On the other hand, when sequences of samples from a single location the seaweed was collected with very young larvae there change in allele frequency from one generation to may have been some truncation of the emergence the next q, should be related to the starting allele period due to sub-optimal laboratory conditions, such as the build up of waste products or predator frequency. As all samples are likely to be at populations. This could cause under-representa- frequencies close to equilibrium, there should be tion of the slow developing aa karyotype.
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