Since the 1980s, it has been known that thyroid hormones are required for migration in birds, including the migratory behaviour itself and the associated physiological preparation. After thyroidectomy, a suite of migratory phenotypes, including the nocturnal restlessness (zugunruhe), pre-migratory fattening (e.g., fat deposition and body mass gain), and feather (re-)generation were all abolished, while TH administration largely restored these phenotypes. Despite these strong evidences, these experiments cannot explain why in some species, migration is a facultative life-history strategy that some populations, or even some individuals in a population, perform it, while other populations/individuals do not. Using two colonies of alpine-breeding Asian House Martins (Delichon dasypus) that are considered partially migratory, we aim to decipher the genomic and hormonal mechanisms underlying their plastic migration strategies. This project is funded by the Grand Challenge Seed Grant from the Academia Sinica, Taiwan.
Thyroid hormones (THs) play crucial roles on embryonic development, growth, metabolism, and life-stage transition. This Academy of Finland (2020-2023) funded project aims to study the potentially complex relationships between THs and the diverse life histories across vertebrates. At the inter-specific level, this project will employ phylogenetic comparative methods to analyse blood TH concentrations across non-domesticated vertebrates. At the intra-specific level, I will also use the long-term monitored common terns (Sterna hirundo) by the Institute of Avian Research, Germany, to tackle how variation in blood THs may be associated with variation in their growth, physiology, and life-history traits. We have finished the hormone analysis for this project, stay tuned for the results in the near future!
Adult blood TH variation Starting with birds, we set out to compile published data of blood TH concentrations and examine which life-history traits might be able to explain part of the inter-specific variation in THs. As changes in life histories likely required accompanying physiological changes, we hope this project will shed light on the macroevolutionary patterns between THs and life-history variation.
TH ontogenetic variation By collaborating with multiple research teams, I am also aiming to look at the ontogenetic patterns of the thyroid along the entire altricial-precocial spectrum in birds. As in birds, the altricial developmental mode appears after the precocial developmental mode, this project might provide information to generate hypotheses that may explain the evolution of altriciality.
THs versus life-history trait variation and reproductive performance Making use of the blood samples collected over years, we aim to explore the potential relationships between TH physiology, life-history trait variation, and reproductive performance in the long-lived common terns (Sterna hiruno) breeding at Banter See, Wilhelmshaven, Germany.
Maternal hormone induced developmental and phenotypic plasticity
Over the past decades, hormones of maternal origin have been recognized as potent mediators to induce developmental and phenotypic plasticity in the offspring. During early pregnancy or egg formation, various hormones are transferred to developing embryos from the mother either across the placenta in viviparous animals or deposited in the egg yolks in oviparous animals. While such hormone-mediated maternal effects have been generally recognized to have profound impact on offspring phenotype and bring about fitness consequences, empirical studies have realized more and more inconsistent results, implying the existence of other modulators. Despite the potential of maternal effects to speed up or constrain the rate of trait evolution, their adaptive significance is still in debate. Moreover, the fitness interest between mothers and offspring may not always be in agreement, leaving room for mother-embryo conflict. To date, the underlying physiological and molecular mechanisms of maternal-hormone transfer, and their actions on embryos remain elusive. Hence, many questions regarding the evolutionary significance of maternal hormones and hormone-induced plasticity remain unanswered and require more delicate approaches to tackle.
Context-dependent effects of maternal yolk hormones
In order to understand the fitness consequences of maternal hormones, studies that experimentally elevated yolk hormones to mimic higher maternal transfer have been conducted in many oviparous animals, predominantly in birds. However, instead of shedding light on its function, these efforts yield more and more inconsistent results, largely thwarting further advancement to our understanding. Because of their well-known pleiotropic effects, hormones may induce different final outcomes depending on the prenatal and postnatal environmental context. Although this possibility has been proposed in early 2000s, empirical evidence either to support or reject it remains highly limited. Such context dependency likely also occurs for non-environmental factors and should be broadly defined. Using several avian model systems, I study the context-dependent effects of maternal testosterone and thyroid hormones:
External environment: food availability Traditionally, higher levels of yolk androgens, including testosterone (T), androstenedione (A4), and dihydrotestosterone (DHT), are considered able to increase metabolism and growth and stimulate begging and aggressive behaviour, which should therefore incur a higher energetic requirement. A commonly reported negative effect of exposure to elevated androgens is suppressed immune function. If an individual was to compensate for this, more energy is thus required to mount appropriate immune responses. All these suggest that energetic balance might determine the final outcome of prenatal androgen exposure. In the wild, food availability directly decides the status of energetic trade-off. A study in spotless starlings (Sturnus unicolor) indeed found that only among the second broods in a season, when food availability declines, nestlings from androgen-injected eggs suffered higher mortality. Such a food-dependent effect of maternal yolk androgen may also work in concert with hatching asynchrony, another maternal effect induced by mothers beginning to incubate before clutch completion, and optimize the number of offspring for the mother according to the available resources. To this end, we have used rock pigeons (Columba livia) as a model system. Making use of the natural difference in yolk androgen levels between the two eggs of a clutch, we want to test whether food availability alone might lead to opposite effects of elevated yolk testosterone. If this is the case, selection may have favored co-evolution between the two maternal effects.
External environment: temperature Thyroid hormones (THs) play an important role in the development of thermoregulation. Maternally-transferred THs therefore might serve important functions for altricial birds because their offspring are not able to thermoregulate themselves during the early postnatal period and require extensive parental brooding. Although the presence of maternally derived THs in avian egg yolks has been confirmed around 1990s, their function in an eco-evolutionary context has been largely understudied. By in ovo injection of THs, several recent studies suggest biologically relevant effects of yolk THs on offspring phenotype, but apparently different results were already observed in different species. In the collared flycatchers (Ficedula albicollis), we found transient growth-enhancing effects during the early postnatal period, but in its sister species, the pied flycatchers (Ficedula hypoleuca), such effects were not observed. We therefore designed a series of experiments, combining yolk TH injection and nest-box temperature treatment (heating or cooling), to study the potential temperature-dependent effects of yolk THs in a couple of nest-box breeding passerines.
Internal environment: interactive relationships among egg substances For lecithotrophic species, the egg, particularly the egg yolk, provides everything the embryo needs to develop until hatching. The egg therefore constitutes the direct environment that is vital for the developing embryo. Such an environment is by no means simple, but composed of various maternally-derived substances, including nutrients, hormones, antioxidants, anti-microbial agents, etc. Imaginably, different egg components likely influence embryonic development in a complex and interactive way. Attempting to unravel how multiple egg substances interactively influence offspring phenotype is, however, highly challenging, and such studies are therefore still in an infancy. The rock pigeon, with the natural within-clutch difference in yolk androgens, provides a handy study system that manipulating one substance can conveniently create a 2-by-2 design to test whether yolk androgens have interactions with other egg substance to shape offspring phenotype.
Ecological and physiological determinants of variation in maternal yolk hormones
Intraspecific variation For maternal hormones to be a tool that mothers can use to maximize her fitness return, animals must possess the plasticity to adjust hormone transfer/deposition. Observing this, however, is not an easy task, as the variation in maternal yolk hormones is always subject to various sources of influence. More complicated is the variation pattern may manifest differently at different levels of biological organizations. To tackle this question, I used both experimental and modelling approaches in both captive and wild study systems. Experimental manipulations are useful in determining whether a certain candidate factors, such as food, may have causal influence on maternal hormone transfer, or in disentangling the underlying physiological mechanisms of hormone transfer. Modern mixed-effects models are particularly powerful and flexible, provided that sufficient data can be gathered, to comb through the complex relationships between yolk hormones and various environmental factors, and to partition different variance components, in a natural set-up.
Main collaborators: Suvi Ruuskanen, Ton Groothuis, Tom Sarraude
Lingering early-life effects on later life: unshakable past?
Prenatal or postnatal, the conditions during early-life period can have profound impact that last through the later life of an individual. Here I broadly and inclusively define "early-life factors" as all environmental and non-environmental factors of various origins (parental, internal, or external) that an individual may encounter during the early stage of life (prenatal or postnatal). Carry-over effects of early-life factors have been well-documented in all kinds of animals, even plants, which may deliver fitness advantages or disadvantages independently of the later-life conditions (i.e. the silver-spoon hypothesis) or interact with anticipatory cue or mediators from the parental generation (e.g. match-mismatch hypothesis). The carry-over effects of early-life condition might even add on top of the interaction between parental and offspring environment. Along with the experiments attempted to test context-dependent effects of maternal hormones, we also examine whether the manipulated early-life factors bring about long-lasting effects on morphology, physiology, behaviour, and survival at a later stage of life.