Environmental correlates of inversion frequencies in natural populations of seaweed flies (Coelopa frigida)

Abstract

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.

Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation?

“…Changes in inversion frequencies were often interpreted in terms of inversion heterozygote advantage, particularly as an excess of heterokaryotypes was found in several population samples. This pattern has also been observed in population samples of Anopheles gambiae mosquitoes (Brooke et al 2002) and Coelopa frigida flies (Butlin & Day 1989). …”

“…In blackflies and seaweed flies, they influence development time. In seaweed flies they also influence size and viability, although trait effects vary with environmental conditions including density (Butlin & Day 1989). Chromosome inversions also influence sperm displacement in seaweed flies; when females mate rapidly with males carrying the same or different karyotypes, sperm from males with the opposite karyotype to the female are favored, resulting in a higher number of heterokaryotypic offspring (Blyth & Gilburn 2005).…”

The genetic effects of competition in seaweed flies

“…Predation by birds certainly occurs, but we have no evidence to suggest that it is selective with respect to the afl inversion system. In contrast, adverse physical conditions do result in differential mortality (Day et al, 1983;Butlin & Day, 1989), with heterokaryotypes exhibiting the highest fitness. The present study showed that larval competition results in a similar pattern of mortality to these climatic factors, which will make it extremely difficult to distinguish their effects.…”

“…The Adh-B allele is always associated with the a form of the inversion, and the D allele with the p form. This genetic polymorphism is stable both temporally and spatially (Day et al, 1983;Butlin & Day, 1989), and is maintained as a result of the superior fitness of as heterokaryotypes; in almost all samples taken from natural populations there is a significant excess of heterokaryotypes over Hardy-Weinberg expectations (Butlin et al, 1982: Day et al, 1983Gilburn & Day, 1994). Preliminary evidence from laboratory culture suggested that the excess of heterokaryotypes increases with larval density .…”

Female mating preference for large size in Coelopa frigida (seaweed fly)

“…One such character is adult size. The phenotypic variation in adult size is very much greater in males than females (Butlin et al, 1982a,b;Day et a!., 1982), and it is the largest males that consistently exhibit the lowest survival from egg to adult (Collins, 1978;Butlin et al, 1982aButlin et al, , 1984Butlin & Day, 1989). A very much weaker candidate to be the preferred character is the genotype at the Adh locus, which was used by Engelhard et al (1989) andFoster (1989) to study male mating success.…”