Annual cycles of metabolic rate are genetically determined but can be shifted by phenotypic flexibility

Versteegh, Maaike A.; Helm, Barbara; Gwinner, Eberhard; Tieleman, B. Irene

doi:10.1242/jeb.073445

Cited by 12 publications

(15 citation statements)

References 63 publications

(102 reference statements)

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“…In contrast, when activation of breeding phenology is entirely plastic, populations in phenological asynchrony would have lower limitations to gene flow. Existing data are insufficient to determine whether differences in breeding timing between conspecific populations of birds generally reflects adaptive and genetic-based specialization or phenotypic plasticity (Nussey et al 2005;Charmantier and Gienapp 2014), although evidence exists for locally adapted cue-integration systems (Hahn and MacDougallShackleton 2008) and for high heritability in circannual rhythms (Hendry and Day 2005;Nussey et al 2005;Versteegh et al 2012). For instance, experiments involving translocation of individuals and monitoring of their breeding behavior have shown reduced fitness when individuals from populations breeding in asynchrony are grouped in the same place (Helm 2009; but see Martin et al 2014).…”

Section: Discussionmentioning

confidence: 99%

Asynchrony of Seasons: Genetic Differentiation Associated with Geographic Variation in Climatic Seasonality and Reproductive Phenology

Quintero

González‐Caro

Zalamea

et al. 2014

The American Naturalist

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. abstract: Many organisms exhibit distinct breeding seasons tracking food availability. If conspecific populations inhabit areas that experience different temporal cycles in food availability spurred by variation in precipitation regimes, then they should display asynchronous breeding seasons. Thus, such populations might exhibit a temporal barrier to gene flow, which may potentially promote genetic differentiation. We test a central prediction of this hypothesis, namely, that individuals living in areas with more asynchronous precipitation regimes should be more genetically differentiated than individuals living in areas with more similar precipitation regimes. Using mitochondrial DNA sequences, climatic data, and geographical/ecological distances between individuals of 57 New World bird species mostly from the tropics, we examined the effect of asynchronous precipitation (a proxy for asynchronous resource availability) on genetic differentiation. We found evidence for a positive and significant cross-species effect of precipitation asynchrony on genetic distance after accounting for geographical/ecological distances, suggesting that current climatic conditions may play a role in population differentiation. Spatial asynchrony in climate may thus drive evolutionary divergence in the absence of overt geographic barriers to gene flow; this mechanism contrasts with those invoked by most models of biotic diversification emphasizing physical or ecological changes to the landscape as drivers of divergence.

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Section: Discussionmentioning

confidence: 99%

Asynchrony of Seasons: Genetic Differentiation Associated with Geographic Variation in Climatic Seasonality and Reproductive Phenology

Quintero

González‐Caro

Zalamea

et al. 2014

The American Naturalist

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“…Inheritance of seasonal variation and seasonal traits (e.g. clutch size) has further been documented by crossbreeding and subsequent study of hybrids (Gwinner et al, 1995a;Helm, 2009;Tieleman et al, 2009;Versteegh et al, 2012a). If seasonal variation of constitutive immunity is driven more heavily by genetic components than environmental components, we would expect it to persist in captivity and to differ between subspecies.…”

Section: Introductionmentioning

confidence: 89%

“…Accordingly, organisms have adjusted their life histories and associated physiology to the variability of the environments they live in (Foster and Kreitzman, 2010;Klaassen, 1995;Nelson et al, 2002;Versteegh et al, 2012a). An important physiological system that relates to selfmaintenance and that connects life history traits with environmental factors is the immune system (Ricklefs and Wikelski, 2002;Sheldon and Verhulst, 1996).…”

Section: Introductionmentioning

confidence: 99%

“…metabolic rate, measures of immunity) among these five genotypic groups are well described and remain present in captivity (Gwinner et al, 1995a;Helm, 2009;Helm et al, 2009;Klaassen, 1995;König and Gwinner, 1995;Tieleman, 2007;Tieleman et al, 2009). For a number of traits, seasonal variation has been shown to persist in captivity, to differ between geographical populations, and to be based on underlying, genetically encoded circannual programs (Gwinner, 1999;Helm, 2009;Helm et al, 2009;Versteegh et al, 2012a). Inheritance of seasonal variation and seasonal traits (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Genetic and phenotypically flexible components of seasonal variation in immune function

Versteegh

Helm

Kleynhans

et al. 2014

Journal of Experimental Biology

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Animals cope with seasonal variation in environmental factors by adjustments of physiology and life history. When seasonal variation is partly predictable, such adjustments can be based on a genetic component or be phenotypically flexible. Animals have to allocate limited resources over different demands, including immune function. Accordingly, immune traits could change seasonally, and such changes could have a genetic component that differs between environments. We tested this hypothesis in genotypically distinct groups of a widespread songbird, the stonechat (Saxicola torquata). We compared variation in immunity during 1 year in long-distance migrants, short-distance migrants, tropical residents and hybrids in a common garden environment. Additionally, we investigated phenotypically flexible responses to temperature by applying different temperature regimes to one group. We assessed constitutive immunity by measuring hemagglutination, hemolysis, haptoglobin and bactericidal ability against Escherichia coli and Staphylococcus aureus. Genotypic groups differed in patterns of variation of all measured immune indices except haptoglobin. Hybrids differed from, but were rarely intermediate to, parental subspecies. Temperature treatment only influenced patterns of hemolysis and bactericidal ability against E. coli. We conclude that seasonal variation in constitutive immunity has a genetic component, that heredity does not follow simple Mendelian rules, and that some immune measures are relatively rigid while others are more flexible. Furthermore, our results support the idea that seasonal variability in constitutive immunity is associated with variability in environment and annualcycle demands. This study stresses the importance of considering seasonal variation in immune function in relation to the ecology and life history of the organism of interest.

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“…Common garden experiments in stonechats have also shown that tropical stonechats have lower CORT and resting metabolic rates than stonechats from the Northern hemisphere, and that this latter difference is heritable but sensitive to life-history stage [4, 49, 50, 88, 89]. One study investigated direct relationships between metabolic rates and CORT and found support for associations on the level of population, but not of individuals [50], thus overall supporting the idea of an involvement of CORT in differences of pace of life.…”

Section: Discussionmentioning

confidence: 99%

Baseline and stress-induced levels of corticosterone in male and female Afrotropical and European temperate stonechats during breeding

et al. 2017

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BackgroundLatitudinal variation in avian life histories falls along a slow-fast pace of life continuum: tropical species produce small clutches, but have a high survival probability, while in temperate species the opposite pattern is found. This study investigated whether differential investment into reproduction and survival of tropical and temperate species is paralleled by differences in the secretion of the vertebrate hormone corticosterone (CORT). Depending on circulating concentrations, CORT can both act as a metabolic (low to medium levels) and a stress hormone (high levels) and, thereby, influence reproductive decisions. Baseline and stress-induced CORT was measured across sequential stages of the breeding season in males and females of closely related taxa of stonechats (Saxicola spp) from a wide distribution area. We compared stonechats from 13 sites, representing Canary Islands, European temperate and East African tropical areas. Stonechats are highly seasonal breeders at all these sites, but vary between tropical and temperate regions with regard to reproductive investment and presumably also survival.ResultsIn accordance with life-history theory, during parental stages, post-capture (baseline) CORT was overall lower in tropical than in temperate stonechats. However, during mating stages, tropical males had elevated post-capture (baseline) CORT concentrations, which did not differ from those of temperate males. Female and male mates of a pair showed correlated levels of post-capture CORT when sampled after simulated territorial intrusions. In contrast to the hypothesis that species with low reproduction and high annual survival should be more risk-sensitive, tropical stonechats had lower stress-induced CORT concentrations than temperate stonechats. We also found relatively high post-capture (baseline) and stress-induced CORT concentrations, in slow-paced Canary Islands stonechats.ConclusionsOur data support and refine the view that baseline CORT facilitates energetically demanding activities in males and females and reflects investment into reproduction. Low parental workload was associated with lower post-capture (baseline) CORT as expected for a slow pace of life in tropical species. On a finer resolution, however, this tropical-temperate contrast did not generally hold. Post-capture (baseline) CORT was higher during mating stages in particular in tropical males, possibly to support the energetic needs of mate-guarding. Counter to predictions based on life history theory, our data do not confirm the hypothesis that long-lived tropical populations have higher stress-induced CORT concentrations than short-lived temperate populations. Instead, in the predator-rich tropical environments of African stonechats, a dampened stress response during parental stages may increase survival probabilities of young. Overall our data further support an association between life history and baseline CORT, but challenge the role of stress-induced CORT as a mediator of tropical-temperate variation in life history.Electro...

show abstract

Annual cycles of metabolic rate are genetically determined but can be shifted by phenotypic flexibility

Cited by 12 publications

References 63 publications

Asynchrony of Seasons: Genetic Differentiation Associated with Geographic Variation in Climatic Seasonality and Reproductive Phenology

Asynchrony of Seasons: Genetic Differentiation Associated with Geographic Variation in Climatic Seasonality and Reproductive Phenology

Genetic and phenotypically flexible components of seasonal variation in immune function

Baseline and stress-induced levels of corticosterone in male and female Afrotropical and European temperate stonechats during breeding

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