Abstract
In a variable yet predictable world, organisms may use environmental cues to make adaptive adjustments to their phenotype. Such phenotypic flexibility is expected commonly to evolve in life history traits, which are closely tied to Darwinian fitness. Yet adaptive life history flexibility remains poorly documented. Here we introduce the collembolan Folsomia candida, a soil-dweller, parthenogenetic (all-female) microarthropod, as a model organism to study the phenotypic expression, genetic variation, fitness consequences and long-term evolution of life history flexibility. We demonstrate that collembola have a remarkable adaptive ability for adjusting their reproductive phenotype: when transferred from harsh to good conditions (in terms of food ration and crowding), a mother can fine-tune the number and the size of her eggs from one clutch to the next. The comparative analysis of eleven clonal populations of worldwide origins reveals (i) genetic variation in mean egg size under both good and bad conditions; (ii) no genetic variation in egg size flexibility, consistent with convergent evolution to a common physiological limit; (iii) genetic variation of both mean reproductive investment and reproductive investment flexibility, associated with a reversal of the genetic correlation between egg size and clutch size between environmental conditions ; (iv) a negative genetic correlation between reproductive investment flexibility and adult lifespan. Phylogenetic reconstruction shows that two life history strategies, called HIFLEX and LOFLEX, evolved early in evolutionary history. HIFLEX includes six of our 11 clones, and is characterized by large mean egg size and reproductive investment, high reproductive investment flexibility, and low adult survival. LOFLEX (the other five clones) has small mean egg size and low reproductive investment, low reproductive investment flexibility, and high adult survival. The divergence of HIFLEX and LOFLEX could represent different adaptations to environments differing in mean quality and variability, or indicate that a genetic polymorphism of reproductive investment reaction norms has evolved under a physiological tradeoff between reproductive investment flexibility and adult lifespan.
Highlights
All organisms experience environmental variation, and environmental variation is a fundamental ingredient of the evolution of organismal diversity
We address the following questions: (1) How flexible are egg size, clutch size, and maternal reproductive investment in response to sudden changes in dietary and social conditions? (2) Does the degree of flexibility differ between traits? (3) What fitness benefits do reproductive adjustments carry? (4) How much genetic variation is there in the mean and flexibility of reproductive traits? (5) What are the consequences of different amounts of genetic variation in the flexibility of different traits on the genetic correlations observed under different environmental conditions? (6) How did contemporary variation in reproductive flexibility evolve?
Reproductive adjustments confer fitness benefits In order to probe the adaptive significance of reproductive flexibility, we assessed the effect of environmental conditions on maternal reproductive investment and the relation between egg size and juvenile quality
Summary
All organisms experience environmental variation, and environmental variation is a fundamental ingredient of the evolution of organismal diversity. When environmental variation operates on large temporal and/or spatial scales compared to population persistence or dispersion, constant, genetically fixed traits are expected to evolve within populations, and variation to evolve between populations. Fast/short-scale environmental variation can select for life history strategies that consist in genetically determined rules by which single individuals respond to environmental fluctuations. When environmental variation has some degree of predictability, another type of adaptation is expected: ‘phenotypic flexibility’ ( called ‘flexible phenotypic plasticity’ [8], ‘reversible phenotypic plasticity’ [9], ‘facultative adjustment’ [10] and ‘context dependence’ [11,12]), i.e. the rapid adjustment of labile phenotypic traits in response to fast/short scale variation in environmental conditions. Surprisingly little is known, both theoretically and empirically, about the occurrence and evolution of adaptive life history flexibility [13,14,15]
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