Genetic correlations and the evolution of photoperiodic time measurement within a local population of the pitcher-plant mosquito, Wyeomyia smithii

Abstract

The genetic relationship between the daily circadian clock and the seasonal photoperiodic timer remains a subject of intense controversy. In Wyeomyia smithii, the critical photoperiod (an overt expression of the photoperiodic timer) evolves independently of the rhythmic response to the Nanda-Hamner protocol (an overt expression of the daily circadian clock) over a wide geographical range in North America. Herein, we focus on these two processes within a single local population in which there is a negative genetic correlation between them. We show that antagonistic selection against this genetic correlation rapidly breaks it down and, in fact, reverses its sign, showing that the genetic correlation is due primarily to linkage and not to pleiotropy. This rapid reversal of the genetic correlation within a small, single population means that it is difficult to argue that circadian rhythmicity forms the necessary, causal basis for the adaptive divergence of photoperiodic time measurement within populations or for the evolution of photoperiodic time measurement among populations over a broad geographical gradient of seasonal selection. Heredity (2012) 108, 473-479; doi:10.1038/hdy.2011.108; published online 9 November 2011Keywords: linkage; pleiotropy; photoperiodism; circadian rhythmicity; antagonistic selection INTRODUCTION Herein we are concerned with the genetic and evolutionary relationship between the photoperiodic timer that serves to organize seasonal events and the circadian clock that serves to organize daily events in the life histories of animals. 'Only model organisms live in a world of endless summer; most organisms in nature confront a seasonal environment. Fitness in a seasonal environment involves the abilities to exploit the favorable season, to avoid or mitigate the effects of the unfavorable season, and to make a timely transition between the two lifestyles' (Bradshaw et al., 2004). Timing is of the essence. Organisms cannot wait for the onset of winter but must have physiological mechanisms that enable them to prepare for the winter in advance. A wide variety of animals from rotifers to rodents use the length of the day (photoperiod) as an anticipatory cue in preparation for the changing seasons. Examples include the use of day length to cue the seasonal timing of migration in birds, to cue the seasonal timing of reproduction in mammals, and to cue the seasonal timing of diapause (dormancy) in arthropods (Bradshaw and Holzapfel, 2007a). Photoperiodic response is typically determined by exposing animals to a range of day lengths and plotting percent response as a function of hours of light per day to which they were exposed (Figure 1a). Photoperiodic response curves are usually sigmoid in shape and the day length that promotes a response in 50% of a sample population defines the critical photoperiod (hereafter, CPP) that is used as a proxy for the photoperiodic response curve.For more than 75 years, it has been hypothesized that the causal basis of the seasonal photoperiodic timer is controlled by ...

Circadian Rhythms Differ between Sexes and Closely Related Species of Nasonia Wasps

“…A trait related to circadian rhythms in Nasonia is photoperiodism, apparent in the form of diapause induction in short days [15], [44], [45]. Whether the circadian system in insects, apparent in overt circadian rhythms, and photoperiodism rely on a unique genetic system comprising canonical clock genes or whether these affect both phenotypes through different pathways is still unclear [19], [46], [47]. While it is undisputed that both systems share components (i.e.…”

Photoperiodism: The Calendar of Plants

“…Geographic variation in circadian genes should not be extrapolated to photoperiodism, and modern genetic approaches should be used to identify genes involved in photoperiodism (Bradshaw et al 2012;Emerson et al 2009;Bradshaw and Holzapfel 2008;Bradshaw et al 2003). Lankinen and Forsman (2006) do present further data on this line using Drosophila litoralis and Drosophila montana (Lankinen et al 2013) from different latitudes and refer to older publications (see furthermore Koštál 2011;Takeda and Skopik 1997;Skopik and Takeda 1986).…”

Photoperiodic control of diapause induction in the zygaenid moth <em>Thyrassia penangae</em> &ndash; involving day-length measurement

“…3,16 There remains no conclusive evidence defining the photoperiodic control of diapause in insects; in fact, there is an intense controversy regarding Bünning's hypothesis. [17][18][19][20] The genetic and metabolic components of photoperiodic responses vary among insect species, and diapause appears to have evolved independently numerous times, thus, we anticipate that not all photoperiodic clocks of insects will interact with circadian clocks in the same fashion. 21 Our previous experiments on photoperiodic responses under non-24-h light-dark cycle revealed that when the length of photophase exceeded the critical day length (13.5 h), diapause was inhibited effectively regardless of the duration of the accompanying dark component ( Figure 5 in the study by He et al) 13 .…”

“…The central importance of night length was also seen in data for the flesh fly Sarcophaga argyrostoma (Robineau-Desvoidy) 5 in which the incidence of pupal diapause was very low in cycles containing a short night (eg, LD 12:8 and LD 16:8) with non-24-h light-dark cycles in which photophases of 10, 12, 14, and 16 h were combined with different lengths of scotophase of 4-24 h have been carried out on the zygaenid moth Pseudopidorus fasciata (Felder & Felder, 1862), the pine caterpillars Dendrolimus punctatus (Walker), the rice stem borer Chilo suppressalis (Walker), the Asian corn borer Ostrinia furnacalis, and the fall webworm Hyphantria cunea in our laboratory. [6][7][8][9][10] The photoperiodic response curves in these species all showed that the incidence of larval diapause was low or zero in cycles containing a short night (4 and 8 h), but high in cycles containing a long night (12,16,20, and 24 h), regardless of the length of the photophase, indicating that the length of the scotophase plays an essential role in the determination of diapause in these species.…”