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Genetic Differences in Mating Success and Female Choice in Seaweed Flies (Coelopa Frigida)

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Genetic Differences in Mating Success and Female Choice in Seaweed Flies (Coelopa Frigida) Heredity 62 (1989) 123—131 The Genetical Society of Great Britain Received 13 June 1988 Genetic differences in mating success and female choice in seaweed flies (Coelopa frigida) G. Engeihard, Department of Genetics, University of Nottingham, S. P. Foster and Nottingham NG7 2UH, U.K. T. H. Day An association is described in seaweed flies, Coelopa frigida, between the genotype at the alcohol dehydrogenase (Adh) locus and mating success in pairwise mating trials. Significantly higher mating success was observed in females that carried the Adh-C allele, but no association was observed between Adh genotype and male mating success. There was heterogeneity in the success of different combinations of males and females, but only when the female lacked the C allele. Analyses of video recordings indicated that C-bearing females spent longer mounted by males and that they less frequently rejected males. Evidence is presented for mate discrimination by females not carrying a C allele. The significance of there being genetic differences in both mating success and in female discrimination are discussed in the context of previous results on mating behaviour in natural populations. NTRODUCTION on this latter point are experiments showing that the exercise of choice results in increased repro- Darwin'stheory of sexual selection (Darwin, 1871) ductive success in zebra finches (Burley, 1986), proposed that during the mating process males tungara frogs (Ryan, 1983) and seaweed flies compete with one another for females, and females (Crocker and Day, 1987). Mate choice may also choose between the available males. The evidence lead to the production of progeny better able to for male-male competition is convincing in a wide survive under competitive conditions as in fruit diversity of species, but it is only during the last flies (Partridge, 1980) and seaweed flies (Crocker decade that equivalent evidence has been found and Day, 1987). The experimental support for for female choice. Female widowbirds (Andersson, female choice being inherited is more limited. Only 1982), bowerbirds (Borgia eta!., 1985), sedge in the two-spot ladybird beetle, Adalia bipunctata, warbiers (Catchpole, 1987), zebra finches (Burley, does direct evidence exist for a polymorphism with 1986) and pied flycatchers (Read, 1986) all exercise a genetic basis (Majerus et a!., 1982, 1986; choice on the basis of some male attribute. O'Donald and Majerus, 1985; Majerus, 1986), Examples from other animal groups include although convincing indirect evidence has been sticklebacks (Semler, 1971), frogs (Ryan, 1983) obtained in Drosophila melanogaster (Heisler, and several species of insects (see Thornhill and 1984) and the Trinidad guppy, Poecilia reticulata Alcock, 1983). (Breden and Stoner, 1987). We report here an The demonstration that female choice occurs association in seaweed flies between mating suc- is only the first step in understanding how sexual cess, female choice and the possession of a par- selection operates over evolutionary time. This ticular allele at an enzyme-determining locus. problem has been tackled from a theoretical point All populations of the seaweed fly, Coelopa of view in the models of Fisher (1930), O'Donald frigida, are polymorphic for a large inversion on (1980), Lande (1981) and Kirkpatrick (1982). It is chromosome I (Butlin et a!., 1982a; Day et al., clear that for female choice to evolve and be 1983). This chromosomal rearrangement, which maintained, both the preference itself and the pre- involves over 10 per cent of the genome (Aziz, ferred character should be inherited. Furthermore, 1975; Day et a!., 1982), has profound influences there should be some advantage to females being on the flies' biology. The two alternative forms (a choosy which may be manifest as increased fecun- and/3) are associated with differences in develop- dity, or greater survival of the progeny. Bearing ment time (Day eta!.,1980), adult size (Butlin et 124 G. ENGELHARD, S. P. FOSTER AND T. H. DAY al., 1982b), adult longevity (Butlin and Day. 1985) tion was necessary prior to video trials lasting only and larval survival (Butlin et aL, 1984). There is 45 mm. Checks for virginity indicated that in no also differential male mating success between case had any female been fertilized before the start genotypes (Butlin et a!., 1982b; Day et a!., 1987) of trials. and populations exhibit negative assortative mat- The experimental procedures for pairwise mat- ing with respect to the af3inversion(Day and ing trials and for the video recording of mating Butlin, 1987). A recent analysis of mating (Crocker behaviour were those of Crocker and Day (1987) and Day, 1987) suggested that female seaweed flies and Day ei a!. (1988), with the minor modification might be choosing their mates on the basis of that one female and three males were observed in inversion genotype, and that there might, in addi- each trial. Males were distinguishably marked with tion, be an element of male choice. small spots of paint applied to the dorsal surface This study by Crocker and Day used a labora- of the thorax. Just over 100 trials were conducted tory population that had been intentionally bred each using different animals. On the completion to have reduced genetic variation. In particular, of trials, animals were stored at —25°C and sub- the population only included individuals possess- sequently scored for their genotype at the alcohol ing B and D alleles at the alcohol dehydrogenase dehydrogenase (Adh) locus using starch gel elec- locus (Adh). This locus is known to be associated trophoresis (Butlin et a!., 1982a). with the cr/3 inversion system such that BB homozygotes are always aa homokaryotypes, and DD's are always /3/3's (Day et a!., 1982). A third RESULTS allele, Adh-C, is also commonly found in natural Mating success in pair trials populations. Preliminary mating tests involving females carrying at least one C allele suggested Virgin flies were paired at random and the mating that in these cases mating was random. This admit- success of each pair assessed by whether or not ted the possibility that BB, BD and DD animals they produced larvae. After the trial the Adh were mating discriminately, but that BC, CC, and genotypes of both adults were determined. The CD females did not exhibit mate choice. Here we mating success of males, regardless of the females report evidence in support of this interpretation, with which they were paired, revealed no and suggest that, as in ladybirds, there are genetic heterogeneity between genotypes (table 1). In con- differences in female choice. The data derive from trast there were differences in the mating success pairwise mating trials in which the results of of females. B(, CC and CD females were the most Crocker and Day, (1987) are extended to include successful, and if the data from these three the Adh-C allele. Observations of mating genotypes are pooled, there is a highly significant behaviour provide direct evidence that females not difference between the C-bearing genotypes and carrying the Adh-C allele mate in a discriminating the combined non-C's (x=1171;P<0001). A fashion. similar comparison of C and non-C males reveals no difference (x= 048;P =049).It appears that METHODS possession of an Adh-C allele is associated with greater mating success in females, but not males. Animalswere collected from a natural population Is the success of males (or females) dependent at St. Mary's Island on the north-east coast of on the genotypes of the two animals considered England and were used in experiments within two together? The success of each male genotype gen- generations of being collected. The maintenance erally did not vary with differing females, although of cultures in the laboratory has been described DD males were an exception to this (table 2). by Day and Buckley (1980). Adults were collected When male C's were pooled and non-C's were shortly after eclosion and males and females stored pooled, the two sets of data were similar. The separately at 4°C. When required for pair trials reciprocal comparison yielded a strikingly different flies were transferred to fresh seaweed (Fucus ser- result. While the success of B(, CD and CC ratus and F vesiculosus) at 29°C overnight. For femalesdid not vary with the male genotype, there video recording, animals were left for a further was the strong suggestion of heterogeneity between two days before use. Preliminary experiments BB, BD and DD females. Furthermore, showed that sex-isolation for one day resulted examination of the pooled data indicates that suc- in the appropriate level of sexual activity in 5-h cess was homogeneous with C-bearing genotypes, mating trials (appropriate, that is, for analytical but heterogeneous with non-C females. Although purposes), but that a longer period of sex-starva- non-C females are convincingly heterogeneous, GENETIC DIFFERENCES IN FEMALE MATE CHOICE 125 Table IMating success of different genotypes in pair trials Per cent mating success Adh genotype BB BC BD CC CD DD P Males 651 571 583 438 567 566 331 065 No. of trials (83) (42) (503) (16) (90) (228) Females 610 648 538 692 746 521 1541 0009 No. of trials (105) (91) (513) (13) (63) (163) x2 values (in this and all subsequent tests) were calculated from the original numbers of succesful and unsuccessful pairs. Table 2Mating success of different genotypic combinations of males and females Per cent mating success of males when paired with females of the following genotypes Male genotype BD BB DD BC CD CC df P BD 571(261) 500 (58)
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