Insuliini-laadse kasvufaktori 1 ja kortikosterooni seos värvuliste pesapoegade kasvukiiruse ja lennuvõimestumisedukusega

Väitekirja elektrooniline versioon ei sisalda publikatsioone.Evolutsioonilise ökoloogia eesmärgiks on seletada isendite tunnuste - kasvukiirus, kehakaal ja elumus - arenemist just sellisteks nagu need on. Sünnijärgne kasvukiirus on üheks selliseks tunnuseks, mis seostub otseselt isendi ellujäämusega iseseisva elu alguses ja talvitamisel. Kuna looduslikud tingimused on muutlikud, siis peavad loomad olema füsioloogiliselt paindlikud ja muutustega pidevalt kohanema, et säiliks võimalikult kiire kasv antud keskkonnatingimustes. Hormoonid, nagu insuliini-laadne kasvufaktor 1 (IGF-1) ja glükokortikoidid (stressihormoonid), on ühed olulisemad sellise arengulise plastilisuse füsioloogilised vahendajad, kuid nende täpne funktsioon on vabaltelavail loomadel tänaseni suhteliselt halvasti uuritud. Töö peamine eesmärk oli testida IGF-1 ja kortikosterooni (lindude peamine glükokortikoid) funktsioonide arengulist plastilisust muutlikes kasvu- ja toitumistingimustes. Täpsemalt, taheti teada, kuidas need kaks hormooni reguleerivad linnupoegade kasvu, konditsiooni ja ellujäämust pesaperioodil olukorras, kus kasvutingimusi on eksperimentaalselt muudetud. Selleks viidi läbi pesakonna suuruse manipulatsioon ja IGF-1 süstimise eksperiment vabaltelavatel rasvatihastel (Parus major) ja must-kärbsenäppidel (Ficedula hypoleuca). Tulemused näitasid, et paremates toitumistingimustes (vähendatud pesakondade korral) kasvasid pesapojad koorumisjärgselt kiiremini, olid paremas füsioloogilises konditsioonis ja neil oli vahetult enne lennuvõimestumist kõrgem IGF-1 tase, kui halvemates tingimustes (suurendatud pesakondade korral) kasvanud ja kontrollgrupi poegadel. Pesapoegade vereplasma IGF-1 tase oli pesaperioodi keskel, mil poegade kasvukiirus on maksimaalne, kõrgem kui lennuvõimestumiseelsel ajal, mil kasvukiirus on langenud. On märkimisväärne, et lennuvõimestumiseelne IGF-1 tase seostus negatiivselt kasvukiirusega just paremates toitumistingimustes kasvanud pesapoegadel. See seos näitab tõenäoliselt IGF-1 allareguleerimist paremini arenenud poegadel, kes saavutasid optimaalse lennuvõimestumiseelse kehamassi kiiremini. Ilmselt ei ole vaja sellistel poegadel investeerida nii palju kasvu ja struktuursesse suurusesse lennuvõimestumisperioodi lõpu poole kui väiksematel poegadel. Sulgedes sisalduva kortikosterooni tase (mis tõnäoliselt kajastab hormooni keskmist taset kogu sule kasvamise perioodil) ja selle seos pesapoja kasvukiiruse ning lennuvõimestumisedukusega sõltus pesakonna suuruse manipulatsioonist vaid okasmetsas, kus kasvutingimused kaldusid olema halvemad kui lehtmetsas. Täpsemalt seostus sulgedes sisalduva kortikosterooni tase okasmetsas negatiivselt lennuvõimestumisedukusega ja paraboolse kõvera kohaselt kasvukiirusega. Viimasel juhul oli kortikosterooni madala taseme korral kasvukiirus sellega seotud positiivselt, kuid hormooni taseme suurenedes muutus seos negatiivseks. Seos poegade lennuvõimestumiseelse IGF-1 ja sule kortikosterooni tasemete vahel sõltus pesapoegade füsioloogilisest konditsioonist. Nimelt oli nende kahe hormooni tasemete vahel positiivne seos heas konditsioonis pesapoegadel, kes pärinesid vähendatud suurusega pesakondadest ja negatiivne seos halvas konditsioonis pesapoegadel, kes kasvasid suurendatud pesakondades. Väärib märkimist, et IGF-1 ja kortikosterooni tasemete koosmõju oli seotud ka poegade lennuvõimestumisedukusega. Antud töö tulemused näitavad, et värvuliste pesapoegade vereplasma IGF-1 ja sulgedes sisalduva kortikosterooni tasemed varieeruvad vastavalt kasvutingimustele (nt toidu kättesaadavusele). Tõenäoliselt mängivad uuritud hormoonid tähtsat rolli pesahoidjate lindude poegade kohasuse varieeruvuses, seda läbi füsioloogiliste lõivsuhete nende sünnijärgse kasvukiiruse, füsioloogilise konditsiooni ja lennuvõimestumisedukuse regulatsioonis muutlikes keskkonnatingimustes.The central goal of evolutionary ecology is to explain how certain traits, like growth rate, body weight and survival, have evolved to their current values. Postnatal growth rate is an important life-history trait that is directly associated with survival during the transition to independence and in the overwinter period. Since natural conditions constantly change, animals have to be physiologically flexible and forever adapt to the environment to keep the postnatal growth rate in the highest levels possible given the surrounding conditions. Hormones such as insulin-like growth factor 1 (IGF-1) and glucocorticoids (stress hormones) are potentially important mediators of developmental plasticity, although their function is quite poorly understood in free-living animals to date. In this thesis, brood size manipulation and a hormone-injection experiment were conducted in two free-living passerines, the great tit (Parus major) and pied flycatcher (Ficedula hypoleuca), with the main aim to explore the developmental plasticity of IGF-1 and corticosterone (main glucocorticoid in birds) functions in relation to environmental challenges (e.g. changing nutritional conditions). More specifically, the aim was to see how these two hormones are connected with the variability in growth rates, physiological conditions and survival rates of nestlings during the nest-bound period in experimentally manipulated growing conditions. Results showed that nestlings in better nutritional conditions (decreased broods) had increased postnatal growth rate, better body condition and also higher IGF-1 levels prior to fledging than those in worse nutritional conditions (control and enlarged broods). Plasma IGF-1 levels were higher in the middle of the nestling period, when growth rate was most rapid, than in the pre-fledging stage. Interestingly, at the pre-fledging stage, IGF-1 levels were negatively associated with the growth rate of those nestlings that grew in nutritionally better conditions. Compared to less mature nestlings, this indicates an IGF-1 down-regulation in more mature nestlings, that reached optimal fledging mass quicker, and that probably needed to invest less into somatic growth and structural size at the end of the fledging period. Furthermore, it was shown that feather corticosterone (the measure incorporates an integral hormonal profile over a relatively long time period, during which the feather was growing) and its association with growth rate and fledging success were significantly affected by the treatment only in coniferous forests, where growth conditions had a tendency to be poorer than in deciduous forests. More specifically, it was found that feather corticosterone was negatively related to fledging success and unimodally associated with the growth rate in the coniferous habitat. In the latter case, the positive association between growth rate and corticosterone levels became negative as corticosterone levels increased. Lastly, it was shown that the association between levels of IGF-1 prior to fledging and feather corticosterone depended on the physiological condition of nestlings. Namely, there was a positive association between the hormone levels in nestlings from decreased broods, which where in better condition, and a negative association in nestlings from enlarged broods, which were in worse condition. Interestingly, the interaction between levels of IGF-1 and corticosterone was also related to the survival of the nestlings. The results of the current thesis suggest that nestling plasma IGF-1 and integral feather corticosterone levels vary depending on resource (e.g. food) availability. These hormones potentially play an important role in regulating nestling fitness in altricial birds, by mediating physiological trade-offs in the regulation of their postnatal growth rate, physiological condition and fledging success in the stochastic environment

Insulin-like growth factor 1 of wild vertebrates in a life-history context

Broad variation in intra- and interspecific life-history traits is largely shaped by resource limitation and the ensuing allocation trade-offs that animals are forced to make. Insulin-like growth factor 1 (IGF-1), a growth-hormone-dependent peptide, may be a key player in the regulation of allocation processes. In laboratory animals, the effects of IGF-1 on growth- and development (positive), reproduction (positive), and longevity (negative) are well established. We here review the evidence on these effects in wild vertebrates, where animals are more likely to face resource limitation and other challenges. We point out the similarities and dissimilarities in patterns of IGF-1 functions obtained in these two different study settings and discuss the knowledge we need to develop a comprehensive picture of the role of IGF-1 in mediating life-history variation of wild vertebrates

Short- and long-term effects of nutritional state on IGF-1 levels in nestlings of a wild passerine

Growth trajectories of young animals are intimately connected to their fitness prospects, but we have little knowledge of growth regulation mechanisms, particularly in the wild. Insulin-like growth factor 1 (IGF-1) is a central hormone in regulating resource allocation, with higher IGF-1 levels resulting in more growth. IGF-1 levels generally increase in conjunction with nutritional state, but whether IGF-1 levels are adjusted in response to current nutrient availability or to the nutrient availability integrated over a longer term is not well known. We tested for such effects by supplementary feeding the jackdaw (Corvus monedula) nestlings in experimentally reduced or enlarged broods with either water (control) or a food solution; these manipulations have long- and short-term effects on the nutritional state, respectively. Baseline plasma IGF-1 levels were higher in reduced broods. Food supplementation induced an increase in plasma IGF-1 levels measured one hour later, and this effect was significantly more substantial in nestlings in reduced broods. Changes in plasma IGF-1 levels increased with increased retention of the supplementary food, which was higher in reduced broods, explaining the stronger IGF-1 response. Thus, IGF-1 levels respond to short-term variations in the nutritional state, but this effect is amplified by longer-term variations in the nutritional state. We discuss our findings using a graphical model that integrates the results of the two treatments

Data from: Crosstalk between growth and somatic maintenance in young animals

Growing animals face allocation problems whenever receiving suboptimal amounts of resources in very stochastic natural environments, possibly through a trade-off between growth and somatic maintenance. However, the extent to which such a trade-off exists has remained an open question. We used an insulin-like growth factor 1 (IGF-1) injection treatment in free-living pied flycatcher (Ficedula hypoleuca) nestlings to see how IGF-1 levels mediate the development of an antioxidant phenotype via glutathione peroxidase (GPx). Our study showed that IGF-1 levels underlie variation in GPx activity and provides important information for understanding the mechanisms behind the growth variation of passerines

IGF-1 receptor inhibitor OSI-906 reduces growth in nestlings of a wild passerine

Young animals need to grow to a large body size fast to maximise their survival prospects until sexual maturity. However, body size varies substantially in wild populations, and neither the selection pressures maintaining this variation, nor the regulatory mechanisms are well understood. IGF-1 administration has been shown to accelerate growth, but this does not necessarily imply that natural variation in growth rate is IGF-1 dependent. To test the latter we administered OSI-906 to pied flycatcher Ficedula hypoleuca nestlings, which has an inhibitory effect on IGF-1 receptor activity. We performed the experiment in two breeding seasons to test the prediction that blocking the IGF-1 receptor downregulates growth. As predicted, OSI-906 treated nestlings had lower body mass and reached a smaller structural size than siblings receiving a vehicle only, with the mass difference being most profound at the age preceding the highest body mass growth rate. The IGF-1 receptor inhibition effect on growth varied with age and year of study, and we discuss possible explanations. The OSI-906 administration results indicate that natural variation in growth rate is regulated by IGF-1, and constitutes a novel tool to study causes and consequences of growth variation, but details of the underlying mechanism still need to be resolved.</p

Data from: Insulin-like growth factor 1 and life-history evolution of passerine birds

1. Natural selection has generated a diversity of ways in which vertebrates allocate their resources between fundamental life-history traits. The availability of possible evolutionary trajectories of these traits is limited by various genetic, physiological, and phylogenetic constraints. This causes trade-offs due to shared resource pools for, or genetic linkage of, competing traits. The majority of these trade-offs are mediated by hormones and create the variability of phenotypes that can be observed in nature. 2. Insulin-like growth factor 1 (IGF-1) is an evolutionarily conserved peptide, which has been shown to be essential in the regulation of body size, the pattern of reproductive investment and lifespan across a broad taxonomic range of model species in laboratory and domesticated conditions. However, studies addressing corresponding evolutionary hypotheses on a broader scale and in free-living vertebrates are very rare. 3. In this phylogenetic comparative study on free-living passerines (Passeriformes), we explore the way in which plasma IGF-1 levels underlie the evolution of body size and demographic fitness correlates (clutch size, egg weight, lifespan). 4. We showed firstly that IGF-1 levels were positively associated with the body size of passerines, although smaller birds had larger IGF-1-mediated investment into building up their body faster. IGF-1 levels were negatively associated with lifespan of passerines, and more so in birds with smaller body weight. Finally, IGF-1 levels were negatively associated with clutch size in heavier species, and positively associated with egg weight in species with higher body weight and longer duration of parental care. The pattern was opposite in species with smaller body weight and shorter duration of parental care. 5. The described evolutionary framework indicates that variation in IGF-1 levels can be regarded as an important mechanism that may underlie life-history evolution in passerines. IGF-1 could act as a physiological link mediating the inter-regulatory growth–reproduction–lifespan “life-history triangle” on the pace-of-life continuum. Interestingly, body weight and investment into parental care have likely imposed a constraining effect on the IGF-1-mediated co-evolution of demographic fitness traits, such as lifespan or reproductive investment. This has limited the availability of adaptive pathways via which those traits could evolve as passerines diversified

DATA_Lodjak_Magi_2017

Glutathione peroxidase (GPx) activity data of free-living pied flycatcher (Ficedula hypoleuca) nestlings. Data is in an Excel file

Lodjak_2017_IGF-1_data_Dryad

Passerine (63 species) data for life-history traits and IGF-1 level

Data from: Causal link between insulin-like growth factor 1 and growth in nestlings of a wild passerine bird

Life history of animals is strongly linked with the variability in postnatal growth rates, because the ability to achieve necessary body mass early in life is directly connected with the ability to survive and reproduce later in life. Surprisingly, little is known about the physiological mechanisms connecting food availability with the variability of growth in wild animals. We used a hormonal injection treatment in free-living nestlings of the pied flycatcher (Ficedula hypoleuca). In doing this, we aimed to see how their plasma insulin-like growth factor 1 (IGF-1) levels and its mediation of growth rate vary in response to administration of exogenous IGF-1 during the early period of postnatal development. We showed that the levels of IGF-1 as well as growth rate and body size, in terms of body mass and tarsus length, were significantly higher in IGF-1-injected nestlings, compared with those in the control group. These differences became especially pronounced from day 7 post-hatch onwards during the 13-day nestling period. Additionally, the proportional investment into growth was more profoundly downregulated in IGF-1-injected nestlings at the end of the nestling period, which achieved fledging size earlier, compared with control nestlings. Our results are the first to highlight IGF-1 as the causal link between growth conditions and variability of growth rate and body size in wild vertebrates. Interestingly, the change in IGF-1 levels also showed a plausible, distinct adaptive age- and physical maturity-dependent pattern in nestlings to match the benefits gained by them when investing in growth, with the cost endured during the early days of postnatal development to maximize their fitness. Therefore, this mechanism might be among those mediating the maintenance of genetic variability in growth rates in populations, presumably regardless of the presence of strong directional selection acting upon them

Complex habitat patterns create unpredictable nest predation risk – an artificial nest experiment

Although birds might increase nesting survival by selecting safe sites, nest predation is a major limiting factor in natural bird populations. We investigated how forest structure, predator distribution, and nest location contribute to nest predation risk, and whether lower predation probabilities characterize formerly “safe” sites. We distributed 304 artificial ground and tree nests in a forest landscape, following the previous year locations of forest grouse observations (with and without broods). We modelled nest predation incidence using generalized mixed models; we also identified potential nest predators by tooth/bill marks on plasticine eggs. We found complex habitat effects: nest predation depended non-linearly on the stand age (low risk in post-clear-cut stands; peak values in middle-aged stands) and there were no simple relationships with predator proximity or nest concealment. Predation probabilities were higher in tree nests than in ground nests, and did not differ in the locations where broods had been observed or not