Latitudinal clines: an evolutionary view on biological rhythms

Abstract

Properties of the circadian and annual timing systems are expected to vary systematically with latitude on the basis of different annual light and temperature patterns at higher latitudes, creating specific selection pressures. We review literature with respect to latitudinal clines in circadian phenotypes as well as in polymorphisms of circadian clock genes and their possible association with annual timing. The use of latitudinal (and altitudinal) clines in identifying selective forces acting on biological rhythms is discussed, and we evaluate how these studies can reveal novel molecular and physiological components of these rhythms.

Keywords: circadian; circannual; diapause; latitude; photoperiod; reproduction.

Figure 1.

Annual patterns of (a) twilight duration, (b) photoperiod and (c) temperature, for different latitudinal ranges. (a) Twilight duration for Northern Hemisphere, defined as the time between −12° (nautical twilight) and 0° solar altitude (approx. 20–80% of the log light intensity change between midnight and noon). (b) Photoperiod calculation based on civil twilight times at dawn and dusk. Civil twilight (solar altitude 6° below the horizon) is the moment when log light intensity changes most rapidly [3] and is often considered as the time of ‘lights on’ and ‘lights off’ for biological systems. (c) Monthly mean dry bulb air temperatures (mostly between 1960 and 1990) from 873 weather stations around the world obtained from the World Meteorological Organization (http://www.wmo.int), and globally averaged over 10° latitudinal bands. Colours indicate mid-latitude of each band (hemispheres plotted separately).

Figure 2.

Ellipse-like annual PPT curves predict changing photoperiodic responses with changing latitude and altitude. (a) The annual temperature hysteresis leads to an ellipse-like relationship between temperature and photoperiod, with higher temperatures in autumn than in spring (dots indicate the mid-point of each month). The dotted lines (a,b) indicate a hypothetical threshold temperature at 10 °C at which a certain species starts winter dormancy (e.g. diapause), resulting in a shift towards longer critical photoperiod (CPP) earlier in the year when this species moves north. This fundamental process forms the basis for the expectation that latitudinal clines in photoperiodic response mechanisms may exist in nature. (b) Global warming (by 0.5 °C) will shift PPT ellipses up, whereas altitude will shift PPT ellipses down (by 0.649 °C 100 m⁻¹). The photoperiod–diapause reaction norm (and accompanying CPP) is therefore expected to evolve under these environmental selection pressures (latitude, altitude and global warming).

Figure 3.

Latitudinal clines in photoperiodic and circadian timing mechanisms in insects. Latitude (in ° N) correlates with: (a) critical photoperiod for diapause induction (populations above 800 m altitude were excluded); (b) circadian amplitude of overt rhythms in light--dark (LD) using various indices (see text); (c) phase of entrainment in 3 L : 21 D; (d) circadian period in continuous darkness (DD). (a) Brown, Sericinus montelus (pupae) [13]; black, Wyeomyia smithii (larvae) [14]; purple, Bruchidius dorsalis (larvae) [15]; pink, Chrysopa carnea (adult) [16]; turquoise, Homoeosoma electellum (larvae) [17]; khaki, Tetranychus pueraricola (adult) [18]; cyan, Orius sauteri (adult) [19]; dark blue, Acronicta rumicis (larvae) [11]; red, Nasonia vitripennis (larvae; maternally induced) [20]; green, Drosophila montana (adult) [21]; grey, D. phalerata (adult) [22]; blue, D. transversa (adult) [22]. (b)–(d) Khaki, D. melanogaster (oviposition) [23]; blue, D. subobscura (eclosion) [24]; red, D. littoralis (eclosion) [25]; green, D. auraria (eclosion) [26]. Three equatorial regression data points from Allemand & David [23] were not plotted in (b) for axis consistency.