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Sandre-SL-Et-Al-2018-J-Evol-Biol.Pdf doi: 10.1111/jeb.13387 Weak and inconsistent associations between melanic darkness and fitness-related traits in an insect SIIRI-LII SANDRE*, TANEL KAART†, NATHAN MOREHOUSE‡ & TOOMAS TAMMARU* *Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia †Department of Animal Breeding and Biotechnology, Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Tartu, Estonia ‡Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, USA Keywords: Abstract body size; The idea that the fitness value of body coloration may be affected by bio- coloration; chemically mediated trade-offs has received much research attention. For genetic correlation; example, melanization is believed to interact with other fitness-related traits growth rate; via competition for substrates, costs associated with the synthesis of melanin heritability; or pleiotropic effects of the involved genes. However, genetic correlations melanization. between coloration and fitness-related traits remain poorly understood. Here, we present a quantitative-genetic study of a coloration trait correlated to melanin-based cuticular darkness (‘darkness’, hereafter) in a geometrid moth, Ematurga atomaria. This species has considerable variation in larval appearance. We focus on correlations between larval darkness and fitness- related growth performance traits. Both a half-sib analysis and an ‘animal model’ approach revealed moderately high heritabilities of larval darkness and indices of growth performance. Heritability estimates of darkness derived from the animal model were, however, considerably higher than those based on the half-sib model suggesting that the determination of col- oration includes genetic interactions and epigenetic effects. Importantly, on the host plant with the largest sample size, we found no evidence for either genetic or environmental correlations between darkness and growth param- eters. On an alternative host plant, there was some indication of positive genetic and negative environmental correlation between these traits. This shows that respective relationships are environment-specific. Nevertheless, the overall pattern of weak and inconsistent correlations between larval col- oration and growth parameters does not support universal trade-offs between these traits and suggests that physiological costs of producing colour patterns do not necessarily interfere with adaptive evolution of coloration. value of body coloration may also be affected by bio- Introduction chemically mediated trade-offs is more recent (Hill, Evolutionary explanations of animal coloration have 1990; Milinski & Bakker, 1990) but has received much traditionally relied on the benefits provided by different research attention during the past two decades (e.g. appearances during visually mediated behavioural McGraw, 2005; Svensson & Wong, 2011; Roulin, interactions, such as sex recognition (Rutowski, 1981; 2016). Pigments displayed on the animal integument Schultz & Fincke, 2009) or escaping predator attack are thought to often correlate with the bearers’ physio- (Estrada & Jiggins, 2008). The idea that the fitness logical state due to their multiple roles in the organ- isms. As an example, common pigments such as Correspondence: Toomas Tammaru, Institute of Ecology and Earth carotenoids, pterins, flavonoids and melanins are Sciences, University of Tartu, Vanemuise 46, EE-51014 Tartu, Estonia. known to have antioxidant functions (McGraw, 2005; Tel.: +372 5252420; fax: +372 7 375 830; Galvan et al., 2014) which may link them to individual e-mail: [email protected] ª 2018 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY. J. EVOL. BIOL. 31 (2018) 1959–1968 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2018 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1959 1960 S-L. SANDRE ET AL. differences in processes associated with oxidative stress, quantitative-genetic analysis focussed on both genetic such as growth or immune response. Moreover, corre- and environmental correlations between a melaniza- lations between pigmentation and other traits of the tion-related trait and indices of growth performance, all organism may arise due to pleiotropic effects of the of which we consider informative in the context of evo- genes involved in determining colour patterns (Ducrest lutionary ecology of coloration. For example, a positive et al., 2008; Wittkopp & Beldade, 2009; Roulin, 2016). genetic correlation between larval melanization and The degree of melanization has been found to show growth rate would imply that there may be variability phenotypic correlations with fitness-related traits in in ‘overall genetic quality’ between the genotypes, with various animal taxa (Roff & Fairbairn, 2013; Roulin, the ‘better’ ones possessing more resources to invest in 2016). These correlations have been proposed to pri- both better growth performance and melanization. A marily reflect the cost of synthesizing melanin (Talloen negative genetic correlation would be expected if the et al., 2004; Stoehr, 2006; Gonzalez-Santoyo & Cor- genotypes primarily differed in the way how they allo- doba-Aguilar, 2012): synthesis of melanin generates cate resources between growth and pigment synthesis. reactive oxygen and nitrogen species which are poten- In contrast, a positive environmental correlation would tially harmful and need to be neutralized with antioxi- indicate that favourable environmental conditions also dants (Nappi & Ottaviani, 2000; True, 2003). In facilitate a higher level of investment in melanization, addition, for many animals, the availability of melanin and would thereby indicate costliness of the latter. A precursors may be limiting (Veiga & Puerta, 1996; True, negative environmental correlation between melaniza- 2003; Poston et al., 2005), and this limitation can be tion and growth performance would be more problem- exacerbated by trade-offs between the multiple physio- atic to interpret, but might, as one alternative, point logical roles of melanin in the organism (e.g. immune towards an adaptive decision to allocate more resources defence in insects, True, 2003). If the trade-off is based to melanin-based immunological defences when envi- on limiting precursors, among-trait relationships may ronmental quality is poor. In contrast, absence of corre- become environment-specific, as the limiting role of lations between coloration and growth parameters the precursors inevitably varies across environments would support the view that coloration traits are rela- (Morehouse, 2014). Naturally, however, such trade-offs tively autonomous evolutionarily, not being tightly may differ among environments also for a variety of integrated into physiologically based trade-offs deter- other reasons (e.g. Gonzales et al., 1999; Almasi & mining offspring production of the moths. Roulin, 2015). To date, much of respective literature has relied on Materials and methods phenotypic correlations between coloration and other fitness-related traits. However, deeper understanding of Study species the evolutionary significance of these patterns requires investigating whether they are underlain by genetic cor- Ematurga atomaria (Lepidoptera: Geometridae) is a med- relations (Roulin, 2016). Such correlations have, how- ium-sized (about 2.5 cm in wing span) diurnal moth ever, remained poorly characterized. This applies to common in various habitats across the Palaearctic zone. insects in particular, despite the fact that these animals The solitary larvae are highly polyphagous external are especially suitable for respective studies due to both feeders of the leaves of their host plants (Leraut, 2009). the widespread within-species variation in coloration In the study area, the species is most abundant in (e.g. Hazel, 2002; Gotthard et al., 2009; Singh et al., coniferous forests and on peat bogs where, due to their 2009; Valim€ aki€ et al., 2015), and short generation times. abundance, dwarf shrubs from the family Ericaceae The few existing quantitative-genetic studies on insects must serve as primary host plants. There is no evidence which have involved coloration-related traits (Wilson of geographical differences in host preference (Meister et al., 2001; Armitage & Siva-Jothy, 2005; Cotter et al., et al., 2017). 2008; Roff & Fairbairn, 2013) are primarily concerned Larval development consists of five instars and lasts with correlations between melanization and immuno- for about 1.5 months (Vellau et al., 2013), from June to logical parameters, at the expense of paying attention to August in northern Europe, with individuals subse- the more general relationships between coloration and quently overwintering as pupae. The larvae are cryptic, physiologically based correlates of fitness. mimicking parts of their host plants. There is a consid- In the present paper, we report results of a quantita- erable variation in patterning and darkness of the lar- tive-genetic study designed to investigate correlations vae: they range from light green to dark brown in their between coloration and growth performance in Ema- overall appearance. The variation is continuous, but turga atomaria, a geometrid moth with remarkable with some combinations of traits being more common within-species variation in larval appearance (Porter, than others (Sandre et al., 2013). Part of this variation 1997; Sandre et al., 2013). Three generations of the has been found to be based on plastic responses to host moths were reared in the laboratory, with a half-sib plant-related environmental factors
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