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The Genetics of Phenotypic Plasticity in Adult Abdominal Colour Pattern of Eristalls Arbustorum (Diptera: Syrphidae)

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The Genetics of Phenotypic Plasticity in Adult Abdominal Colour Pattern of Eristalls Arbustorum (Diptera: Syrphidae) Heredity 77 (1996) 493—499 Received 27 November 1995 The genetics of phenotypic plasticity in adult abdominal colour pattern of Eristalls arbustorum (Diptera: Syrphidae) MART M. OTTENHEIM*, ANIQUE D. VOLMERt & GRAHAM J. HOLLOWAY tlnstitute of Evolutiona,y and Ecological Sciences, Section of Evolutionary Biology and Systematic Zoology, Leiden University, P0 Box 9516, 2300 RA, Le/den, The Netherlands and School of Animal and Microbial Sciences, AMS Building, University of Reading, Whiteknights, P0 Box 228, Reading RG6 2AJ, U.K Theabdominal colour pattern of Eristalis arbustorum is a plastic character which is heavily influenced by developmental temperature. The present study investigated the form of the reaction norms of amount of abdominal yellow and intensity of the yellow (measured as grey value) on pupal development temperature. The slope of the reaction norm for amount of yellow was steeper in males than in females. The reaction norms for grey value on temperature were nonlinear. Family groups were reared to enable a consideration of the genetics to be made. There were significant family by environment interactions for both characters for both sexes indicating genetic variance for plasticity. Pupal development time is closely correlated with developmental temperature. The relationship between amount of yellow on the abdomen and log pupal development time was curvilinear and fitted a quadratic function well. There was significant among-family variation in the slopes of these lines for females, but not for males, again suggesting genetic variation for plasticity. The results are discussed in relation to the maintenance of genetic variation. Keywords:Eristalis,genetic variation, hoverflies, plasticity, reaction norm. by a genotype across a range of environments. In Introduction this model genetic variation is demonstrated when Manyorganisms live in a seasonal or otherwise fluc- the reaction norms cross. The models can be inter- tuating environment and are regularly exposed to a changeable under specific circumstances (Via et a!., variety of conditions. It often makes evolutionary 1995). sense for an organism to be able to adjust its pheno- The abdominal colour patterns of several hoverfly type to increase its fitness in relation to prevailing species show considerable plasticity (Heal, 1979a,b, conditions. The ability of a single genotype to give 1981; Holloway, 1993). One of the best studied rise to different phenotypes is referred to as pheno- hoverflies in this respect is Eristalis arbustorum (L.) typic plasticity (Bradshaw, 1965). To study the evolu- (Heal, 1981; Holloway, 1993; Ottenheim et at., tion and genetics of plasticity, two models have been 1995). When the pupa is kept at low temperatures a proposed: the 'character state' approach and the dark colour pattern develops and when it is kept at 'polynomial' approach (Via et at., 1995 and refer- higher temperatures a lighter pattern develops ences therein). In the character state approach a (Heal, 1981; Ottenheim et a!., 1995). As a conse- character is modelled as a set of phenotypic values quence the colour pattern varies over the year with that would be expressed in each environment by a darker forms occurring in the cooler spring months given genotype. Genetic variation for plasticity is and paler forms emerging during the warmer demonstrated by a genotype by environment inter- summer (Holloway, 1993). It has been argued that action (Via & Lande, 1987). In the polynomial this kind plasticity may be adaptive and associated approach, a reaction norm is described by a poly- with the need for the insect to thermoregulate nomial function of the phenotypic values expressed (Heal, 1981; Holloway, 1993). The extent of the pale patterning on the abdomen *Correspondence of E. arbustorum is determined throughout the pupal 1996 The Genetical Society of Great Britain. 493 494 M. M. OTTENHEIM ETAL. stage and, indeed, pupal development time is ensure that at the lower temperatures the larvae strongly correlated with colour pattern size (Otten- would not go into diapause. For each family 20 heim et al., 1995). The wing patterns of many butter- larvae (one tray) were assigned at random to each fly species (e.g. Pieris spp., Polygonia c-album, temperature. Because a higher mortality was Bicyclus spp.) are also plastic characters (Nylin, expected at 8°C (see Ottenheim et al., 1995) another 1989; Kingsolver & Wiernasz, 1991; Windig, 1994). 20 larvae were assigned to this temperature when This plasticity is also often influenced by develop- family size allowed it. ment temperature, particularly during the last larval The colour pattern of E. arbustorum is determined stage and the first few days of pupal development during the pupal stage (Ottenheim et al., 1995). (Nijhout, 1991). This results in some multivoltine Therefore the hatchling larvae were allowed to grow species showing polyphenisms in the field, i.e. each at 20°C for 11 days (i.e. developing into large third generation exhibits a different wing colour pattern. instar larvae) before being transferred to the However, these polyphenisms are generally deter- different temperatures. Using this approach we were mined by hormonal systems which, in their turn, are sure that all flies would experience the experimental influenced by temperature or light regime (Koch, temperatures throughout the whole of their pupal 1992). Considering these findings it is possible that stage. E. arbustorum colour pattern is not influenced by Pupae were collected daily from the larval temperature per se. It is probable that ambient medium and transferred to transparent Petri dishes temperature influences physiologicalprocesses which were kept in full light under the experimental during the pupal phase which determine the amount temperature. Emergent adults were collected daily of yellow on the abdomen. and were kept at 20°C for two days to ensure The purpose of this study was twofold. First, to complete development of the abdominal colour determine the shapes of the reaction norms of two pattern. After 2 days the flies were transferred to a colour pattern characters on the abdomen of E. —20°C freezer for half a day after which they were arbustorum. Secondly, to estimate the degree of dried and sexed. significance of genetic variation for plasticity for the The colour pattern on the abdomen of the adult characters using both the 'character state' and 'poly- flies was quantified using image analysis (see Otten- nomial' approaches described above. heim et al., 1995). The video image of a pinned fly was analysed using the TIM interactive image-analysis software. The flies were measured in several Materialsand methods sessions. Before each session a size calibration was performed. A lightintensity calibration was DuringApril and May 1994, E. arbustorum adults performed before and regularly during each session. were collected in and around Leiden (The Nether- A program was written to indicate natural bound- lands). Egg batches were collected from wild-caught aries on the image on the basis of contrast differ- female flies as described by Ottenheim & Holloway ences resulting in the segmentation of the colour (1995). Newly hatched larvae from each egg batch pattern (for more details see Ottenheim et al., 1995). were initially reared at 20°C before being equally The yellow/brown (hereafter referred to as yellow) and randomly assigned to the experimental tempera- colour pattern of E. arbustorum only appears on the tures (see below). The larval rearing medium was second and third tergites. The characters measured based on rabbit droppings collected from a coastal were the area of yellow on the second tergite, the dune system mixed with water. 20 g yeast (Saccharo- area of yellow on the third tergite, the area of black myces cerivisiae siccum) was added to each litre of on the second tergite and the colour intensity medium to reduce competition between larvae for (average grey value) of the yellow parts on the food. The larvae were bred in small plastic trays second tergite. From this the total area of yellow on (18 x 13 x 4.5 cm) which were separated into two the abdomen and the total area of the second tergite equal compartments and could be closed with a (a measure of abdomen size) were calculated. transparent ventilated lid. In each tray between 14 Because these two characters were phenotypically and 20 larvae were reared in 200 mL medium. correlated (r =0.771and 0.772 for males and To examine the effect of pupal development females, respectively) the residuals of the regression temperature on adult abdominal colour pattern flies of total yellow area on tergite size were used to were reared at six different temperatures: 8, 11, 14, analyse colour pattern size using analysis of 17, 20 and 26°C (all1°C). A light regime of 16 h variance. light and 8 h dark was maintained throughout to To calculate a genotype by environment inter- The Genetical Society of Great Britain, Heredity, 77, 493—499. PHENOTYPIC PLASTICITY IN ER/STALlS ARBUSTORUM 495 action a two-factor analysis of variance was carried analysis of covariance was performed using the GLM out using only those families which had representa- procedure in MINITAB 9.1. tives at all temperatures (,10families; ,9famil- ies). To determine the polynomial relation between Results pupal development time and colour pattern size, the method described by Sokal & Rolf (1994) was Atotal of 1005 flies was obtained of which 516 (51.3 followed. Pupal development time was natural per cent) were female. Overall survival was around logged to correct for non-normality. The overall 40 per cent. Survival was lower at 8 and 11°C than at relation between colour pattern size and pupal the other temperatures. development time was significantly better explained Table 1 summarizes larval and pupal development by a quadratic function (,R=63.1per cent; , times for males and females at the different R2=57.7per cent) than by a linear relationship (6 temperatures. The results of the analyses are R2 =61.8per cent; ,R2=55.5per cent) (: shown in Table 3.
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