Life-history States Research Articles

Effect of Photoperiod and Illuminance on Daily Activity Patterns, Physiology, and NPY Peptide Expression in Migratory Redheaded Buntings (Emberiza bruniceps)

Introduction: Light is the primary source of energy and regulates seasonal changes in physiology and behavior. The role of photoperiod has been much investigated in several bird species, but the role of illumination in seasonal adaptations of passerine finches is less understood. We, therefore, investigated the effects of photoperiod and illuminance on migratory physiology in a Palearctic-Indian migratory finch, redheaded bunting (Emberiza bruncieps). Methods: Photosensitive buntings maintained under short days (8L:16D) were divided into three groups receiving 5, 25, and 100 lux of white daytime illuminance, respectively. Thereafter, using photoperiodic manipulation three life history states, i.e., nonmigratory (NM), premigratory (PM), and migratory (MIG) states were induced in the buntings. The birds in the MIG state were consecutively perfused after seven nights of Zugunruhe (nighttime migratory restlessness) for neuropeptide Y (NPY)-immunohistochemistry, which is involved in a wide range of functions including energy homeostasis, vision, and fat deposition in birds. Results: We found differential effects of illuminance on locomotor activity and physiology. Photostimulated birds showed intense nighttime activity in the MIG state. We observed premigratory hyperphagia in the birds, with increased food intake in the 100 lux group, which was reflected in the body mass gain in the MIG state. NPY expression on the periphery of the nucleus rotundus suggests its potential role in visual acuity, where the NPY-cell count significantly decreased under 25 lux illumination. Conclusion: We demonstrate that migrating birds may also experience physiological effects from changes in daytime illumination. We observed illuminance-dependent variations in the quantity of food consumed by the birds. It indicates that the illuminance may also impact the encephalic centers that control food intake.

Disentangling the influence of entanglement on recruitment in North Atlantic right whales.

North Atlantic right whales are Critically Endangered and declining, with entanglements in fishing gear a key contributor to their decline. Entanglement events can result in lethal and sub-lethal (i.e. increased energetic demands and reduced foraging ability) impacts, with the latter influencing critical life-history states, such as reproduction. Using a multi-event framework, we developed a Bayesian mark-recapture model to investigate the influence of entanglement severity on survival and recruitment for female right whales. We used information from 199 known-aged females sighted between 1977 and 2018, combined with known entanglements of varying severity that were classified as minor, moderate or severe. Severe entanglements resulted in an average decline in survival of 27% for experienced non-breeders, 9% for breeders and 26% for pre-breeding females compared with other entanglements and unentangled individuals. Surviving individuals with severe entanglements had low transitional probabilities to breeders, but surprisingly, individuals with minor entanglements had the lowest transitional probabilities, contrary to expectations underpinning current management actions. Management actions are needed to address the lethal and sub-lethal impacts of entanglements, regardless of severity classification.

Ascorbic acid releases dormancy and promotes germination by an integrated regulation of abscisic acid and gibberellin in Pyrus betulifolia seeds.

Seed dormancy is an important life history state in which intact viable seeds delay or prevent germination under suitable conditions. Ascorbic acid (AsA) acts as a small molecule antioxidant, and breaking seed dormancy and promoting subsequent growth are among its numerous functions. In this study, a germination test using Pyrus betulifolia seeds treated with exogenous AsA or AsA synthesis inhibitor lycorine (Lyc) and water absorption was conducted. The results indicated that AsA released dormancy and increased germination and 20 mmol L-1 AsA promoted cell division, whereas Lyc reduced germination. Seed germination showed typical three phases of water absorption; and seeds at five key time points were sampled for transcriptome analysis. It revealed that multiple pathways were involved in breaking dormancy and promoting germination through transcriptome data, and 12 differentially expressed genes (DEGs) related to the metabolism and signal transduction of abscisic acid (ABA) and gibberellins (GA) were verified by subsequent RT-qPCR. For metabolites, exogenous AsA increased endogenous AsA and GA3 but reduced ABA and the ABA/GA3 ratio. In addition, three genes regulating ABA synthesis were downregulated by AsA, while five genes mediating ABA degradation were upregulated. Taken together, AsA regulates the pathways associated with ABA and GA synthesis, catalysis, and signal transduction, with subsequent reduction in ABA and increase in GA and further the balance of ABA/GA, ultimately releasing dormancy and promoting germination.

Photoperiod-driven concurrent changes in hypothalamic and brainstem transcription of sleep and immune genes in migratory redheaded bunting.

The molecular regulation of sleep in avian migrants is still obscure. We thus investigated this in migratory redheaded buntings, where four life-history states (LHS; i.e. non-migratory, pre-migratory, migratory and refractory states) were induced. There was increased night-time activity (i.e. Zugunruhe) during the migratory state with reduced daytime activity. The recordings of the sleep-wake cycle in buntings showed increased night-time active wakefulness coupled with drastically reduced front and back sleep during migratory phase. Interestingly, we found the buntings to feed and drink even after lights-off during migration. Gene expression studies revealed increased hypothalamic expression of glucocorticoid receptor (nr3c1), and pro-inflammatory cytokines (il1b and il6) in pre-migratory and migratory states, respectively, whereas in brainstem Ca2+/calmodulin-dependent protein kinase 2 (camk2) was upregulated during the migratory state. This suggested a heightened pro-inflammatory state during migration which is a feature of chronic sleep loss, and a possible role of Ca2+ signalling in promoting wakefulness. In both the hypothalamus and brainstem, the expression of melatonin receptors (mel1a and mel1b) was increased in the pre-migratory state, and growth hormone-releasing hormone (ghrh, known to induce sleep) was reduced during the migratory state. The current results demonstrate key molecules involved in the regulation of sleep-wake cycle across LHS in migratory songbirds.

Photoperiodic modulation of melatonin receptor and immune genes in migratory redheaded bunting

The transcriptional regulation of innate immune function across annual life history states (LHS) remains obscure in avian migrants. We, therefore, investigated this in a migratory passerine songbird, redheaded bunting (Emberiza bruniceps), which exhibits long-distance vernal migration from India to Central Asia. We exposed the birds (N = 10) to differential photoperiodic conditions to induce a non-migratory (NM), pre-migratory (PM), migratory (MIG), and refractory (REF) state, and performed gene expression assays of melatonin receptors (MEL1A and MEL1B), and innate immunity-linked genes (IL1B, IL6, TLR4, and NFKB) in spleen and blood. We found a significant reduction in splenic mass and volume, and a parallel increase in fat accumulation, and testicular growth in birds under migratory state. The gene expression assay revealed an upregulation of MEL1A and MEL1B mRNA levels in both the tissues in MIG. Additionally, we found a nocturnal increase of splenic IL1B expression, and IL1B, IL6, and TLR4 expression in the blood. The mRNA expression of melatonin receptors and proinflammatory cytokine showed a positive correlation. These results suggest that melatonin relays the photoperiodic signal to peripheral immune organs, which shows LHS-dependent changes in mRNA expression of immune genes.

Control and adaptability of seasonal changes in behavior and physiology of latitudinal avian migrants: Insights from laboratory studies in Palearctic-Indian migratory buntings.

Twice-a-year migrations, one in autumn and the other in spring, occur within a discrete time window with striking alterations in the behavior and physiology, as regulated by the interaction of endogenous rhythms with prevailing photoperiod. These seasonal voyages are not isolated events; rather, they are part of an overall annual itinerary and remain closely coupled to the other annual subcycles, called seasonal life history states (LHSs). The success of migration depends on appropriate timing of the initiation and termination of each LHS, for example, reproduction, molt, summer nonmigratory, preautumn migratory (fattening and weight gain), autumn migratory, winter nonmigratory (wnM), prevernal (spring) migratory (fattening and weight gain), and spring migratory LHSs. Migration-linked photoperiod-induced changes include the body fattening and weight gain, nocturnal Zugunruhe (migratory restlessness), elevated triglycerides and free fatty acids, triiodothyronine and corticosterone levels. Hypothalamic expression of the thyroid hormone-responsive dio2 and dio3, light-responsive per2, cry1,and adcyap1 and th (tyrosine hydroxylase, involved in dopamine biosynthesis) genes also show significant changes with transition from wnM to the vernal migratory LHS. Concurrent changes in the expression of genes associated with lipid metabolism and its transport also occur in the liver and flight muscles, respectively. Interestingly, there are clear differences in the behavioral and physiological phenotypes, and associated molecular changes, between the autumn and vernal migrations. In this review, we discuss seasonal changes in the behavior and physiology, and present molecular insights into the development of migratory phenotypes in latitudinal avian migrants, with special reference to Palearctic-Indian migratory buntings.

Comparisons of cell proliferation and cell death from tornaria larva to juvenile worm in the hemichordate Schizocardium californicum

BackgroundThere are a wide range of developmental strategies in animal phyla, but most insights into adult body plan formation come from direct-developing species. For indirect-developing species, there are distinct larval and adult body plans that are linked together by metamorphosis. Some outstanding questions in the development of indirect-developing organisms include the extent to which larval tissue undergoes cell death during the process of metamorphosis and when and where the tissue that will give rise to the adult originates. How do the processes of cell division and cell death redesign the body plans of indirect developers? In this study, we present patterns of cell proliferation and cell death during larval body plan development, metamorphosis, and adult body plan formation, in the hemichordate Schizocardium californium (Cameron and Perez in Zootaxa 3569:79–88, 2012) to answer these questions.ResultsWe identified distinct patterns of cell proliferation between larval and adult body plan formation of S. californicum. We found that some adult tissues proliferate during the late larval phase prior to the start of overt metamorphosis. In addition, using an irradiation and transcriptomic approach, we describe a genetic signature of proliferative cells that is shared across the life history states, as well as markers that are unique to larval or juvenile states. Finally, we observed that cell death is minimal in larval stages but begins with the onset of metamorphosis.ConclusionsCell proliferation during the development of S. californicum has distinct patterns in the formation of larval and adult body plans. However, cell death is very limited in larvae and begins during the onset of metamorphosis and into early juvenile development in specific domains. The populations of cells that proliferated and gave rise to the larvae and juveniles have a genetic signature that suggested a heterogeneous pool of proliferative progenitors, rather than a set-aside population of pluripotent cells. Taken together, we propose that the gradual morphological transformation of S. californicum is mirrored at the cellular level and may be more representative of the development strategies that characterize metamorphosis in many metazoan animals.

Machine learned daily life history classification using low frequency tracking data and automated modelling pipelines: application to North American waterfowl

BackgroundIdentifying animal behaviors, life history states, and movement patterns is a prerequisite for many animal behavior analyses and effective management of wildlife and habitats. Most approaches classify short-term movement patterns with high frequency location or accelerometry data. However, patterns reflecting life history across longer time scales can have greater relevance to species biology or management needs, especially when available in near real-time. Given limitations in collecting and using such data to accurately classify complex behaviors in the long-term, we used hourly GPS data from 5 waterfowl species to produce daily activity classifications with machine-learned models using “automated modelling pipelines”.MethodsAutomated pipelines are computer-generated code that complete many tasks including feature engineering, multi-framework model development, training, validation, and hyperparameter tuning to produce daily classifications from eight activity patterns reflecting waterfowl life history or movement states. We developed several input features for modeling grouped into three broad categories, hereafter “feature sets”: GPS locations, habitat information, and movement history. Each feature set used different data sources or data collected across different time intervals to develop the “features” (independent variables) used in models.ResultsAutomated modelling pipelines rapidly developed easily reproducible data preprocessing and analysis steps, identification and optimization of the best performing model and provided outputs for interpreting feature importance. Unequal expression of life history states caused unbalanced classes, so we evaluated feature set importance using a weighted F1-score to balance model recall and precision among individual classes. Although the best model using the least restrictive feature set (only 24 hourly relocations in a day) produced effective classifications (weighted F1 = 0.887), models using all feature sets performed substantially better (weighted F1 = 0.95), particularly for rarer but demographically more impactful life history states (i.e., nesting).ConclusionsAutomated pipelines generated models producing highly accurate classifications of complex daily activity patterns using relatively low frequency GPS and incorporating more classes than previous GPS studies. Near real-time classification is possible which is ideal for time-sensitive needs such as identifying reproduction. Including habitat and longer sequences of spatial information produced more accurate classifications but incurred slight delays in processing.

Seed dormancy in space and time: global distribution, paleoclimatic and present climatic drivers, and evolutionary adaptations.

Seed dormancy is an important life history state that increases survival and fitness of seed plants, and thus it has attracted much attention. However, global biogeography, effects of paleoenvironment, evolutionary roles of dormancy transitions, and differences in adaptations of seed dormancy between life-forms are poorly understood. We compiled global distribution records for seed dormancy of 12 743 species and their phylogeny to explore the biogeographic patterns, environmental drivers, and evolutionary transitions between seed dormancy and nondormancy. Biogeographic patterns reveal a low proportion of dormancy in tropical rainforest regions and arctic regions and a high proportion of dormancy in remaining tropical, subtropical, and temperate regions for all species and woody species. Herbaceous plants show a greater proportion of dormancy in most global regions except arctic regions. Seasonal environments have a consistent positive influence on the dormancy pattern for both life-forms, but precipitation and temperature were important driving factors for woody and herbaceous plants, respectively. Seed dormancy was the dominating state during the evolutionary history of seed plants, and dormancy transitions had a significant relationship with paleotemperatures. Dormancy and nondormancy transitions in response to fluctuating environments during long-term evolutionary history may have played important roles in the diversification of seed plants. Our results add to the current knowledge about seed dormancy from macro-adaptive perspectives and the potential adaptive mechanisms of seed plants.

Complex tourism and season interactions contribute to disparate physiologies in an endangered rock iguana.

To promote survival and fitness, organisms use a suite of physiological systems to respond to both predictable and unpredictable changes in the environment. These physiological responses are also influenced by changes in life history state. The continued activation of physiological systems stemming from persistent environmental perturbations enable animals to cope with these challenges but may over time lead to significant effects on the health of wildlife. In the present study, we tested how varying environmental perturbations driven by tourism and associated supplemental feeding affects the energetics, corticosterone and immunity of six discrete populations of the northern Bahamian rock iguana (Cyclura cychlura inornata and Cyclura cychlura figginsi). We studied populations within and outside the reproductive season and quantified tourist numbers during sample collection. Specifically, we measured clutch size, body condition, plasma energy metabolites, reactive oxygen species, baseline corticosterone concentrations and immune function of male and female iguanas from each population to address whether (i) disparate physiologies are emerging across a gradient of tourism and feeding, (ii) both subspecies respond similarly and (iii) responses vary with season/reproductive condition. We found significant effects of tourism level, season and their interaction on the physiology of both C. c. inornata and C. c. figginsi, supporting the idea that tourism is leading to the divergence of phenotypes. Specifically, we found elevated plasma energy metabolites, oxidative stress and a measure of innate immunity (bactericidal ability), but reduced corticosterone concentrations with increasing tourism in both subspecies of rock iguanas. These physiological metrics differ according to the level of tourism in both subspecies and persist across seasons despite variation with natural seasonal and reproductive changes. These findings suggest that anthropogenic disturbance results in disparate physiologies in northern Bahamian rock iguanas.

Differences in transcription regulation of diurnal metabolic support to physiologically contrasting seasonal life-history states in migratory songbirds

Differences in transcription regulation of diurnal metabolic support to physiologically contrasting seasonal life-history states in migratory songbirds

Photoperiodically driven transcriptome-wide changes in the hypothalamus reveal transcriptional differences between physiologically contrasting seasonal life-history states in migratory songbirds

We investigated time course of photoperiodically driven transcriptional responses in physiologically contrasting seasonal life-history states in migratory blackheaded buntings. Birds exhibiting unstimulated winter phenotype (photosensitive state; responsive to photostimulation) under 6-h short days, and regressed summer phenotype (photorefractory state; unresponsiveness to photostimulation) under 16-h long days, were released into an extended light period up to 22 h of the day. Increased tshβ and dio2, and decreased dio3 mRNA levels in hypothalamus, and low prdx4 and high il1β mRNA levels in blood confirmed photoperiodic induction by hour 18 in photosensitive birds. Further, at hours 10, 14, 18 and 22 of light exposure, the comparison of hypothalamus RNA-Seq results revealed transcriptional differences within and between states. Particularly, we found reduced expression at hour 14 of transthyretin and proopiomelanocortin receptor, and increased expression at hour 18 of apolipoprotein A1 and carbon metabolism related genes in the photosensitive state. Similarly, valine, leucine and isoleucine degradation pathway genes and superoxide dismutase 1 were upregulated, and cocaine- and amphetamine-regulated transcript and gastrin-releasing peptide were downregulated in the photosensitive state. These results show life-history-dependent activation of hypothalamic molecular pathways involved in initiation and maintenance of key biological processes as early as on the first long day.

Stress and reproductive events detected in North Atlantic right whale blubber using a simplified hormone extraction protocol.

As studies quantifying steroid hormones in marine mammal blubber progress, methodological refinements may improve the utility and consistency of blubber hormone measurements. This study advances blubber extraction methodologies by testing a simplified extraction protocol that reduces time and complexity compared to a protocol widely used in cetacean blubber studies. Using blubber samples archived from remote biopsy (n = 21 live whales) and necropsy collection (n = 7 dead whales) of North Atlantic right whales (NARW; Eubalaena glacialis) of known life history states, we performed analytical and biological validations to assess the feasibility of measuring reproductive (testosterone, progesterone) and glucocorticoid (cortisol) hormones in blubber via enzyme immunoassay following the simplified extraction. Analytical validations (parallelism, accuracy, extraction efficiency, repeatability) showed the simplified extraction produced similar results to the extended protocol, offering a more efficient and consistent technique. In live, apparently healthy whales, blubber testosterone concentrations (mean ± SE) were significantly higher in males (2.02 ± 0.36ng/g) compared to females (0.81 ± 0.15ng/g). Blubber progesterone was highest in a confirmed pregnant female (60.3ng/g), which was 12-fold greater than the mean concentration of non-pregnant females (4.56 ± 0.88ng/g). Blubber cortisol concentrations in whales that died from anthropogenic causes averaged 5.31 ± 2.28ng/g, whereas most live, healthy whales had cortisol values below 1ng/g. Among living whales, a whale actively entangled in fishing gear had the highest blubber cortisol measurement (3.51ng/g), exhibiting levels similar to whales that died from acute entanglement (2.88 ± 0.42ng/g). Overall, the highest blubber cortisol concentration (18.0ng/g) was measured in a dead whale with a severe chronic entanglement, approximately 30-fold greater than mean blubber cortisol of apparently healthy whales (0.58 ± 0.11ng/g). The methodological approach presented here provides a reference for researchers interested in an alternative, streamlined technique for hormone extraction of cetacean blubber and contributes to the diverse tool set for stress and reproductive assessments of endangered NARWs.

Determinism of Temporal Variability in Size at Maturation of Sardine Sardina pilchardus in the Bay of Biscay

Age and size at maturation appear as key parameters governing the dynamics of a population as they affect growth rate, fecundity, and survival. The expression of such life history traits is determined by genetic make-up and modulated by environmental factors mainly through phenotypic plasticity. Moreover, fishing, besides decreasing population size and changing demographic composition can alter allelic frequencies through fisheries-induced evolution by selecting for some particular traits. In the Bay of Biscay, a decreasing trend in both sardine body condition and size-at-age has recently been pointed out at the population level. The Probabilistic Maturation Reaction Norm (PMRN) approach was applied to help disentangle phenotypic plasticity and genetic changes. Based on the analysis of sardine spawning seasonality, PMRN was estimated by considering body condition as additional life-history state variable to predict the onset of maturation. The resulting PMRN was then used to investigate temporal trends in reaction norm midpoints to test whether changes in length at maturation can be explained by plastic and/or evolutionary adaptive change. Overall, our results emphasize for the first time that including sardine body condition as explanatory variable improves predictions of maturation probability. We found that better individual condition increases maturation probability. The assessment of temporal changes in length at maturation confirms the low plasticity in this trait for a species maturing mostly at age-1 and advocates for the use of a monthly time scale when investigating PMRNs for this species. Beside environmental variables included in this analysis (water temperature, chlorophyll-a, and population biomass) that only show a weak correlation with PMRN midpoints, our results reveal no evidence for recent fisheries-induced evolution in the sardine stock of the Bay of Biscay. They suggest that the short-term variability in length at maturation is strongly dependent upon individual growth which is likely driven by environmental factors. For sardine fisheries management, our study highlights the need to consider both the length-composition data and the seasonality within a stock assessment model. Finally, we discuss the fact that considering individual growth trajectories should improve our understanding of the relationship between environmental variability and changes in maturation for sardine.

Migration gives sleepless nights to the birds: a study on a Palaearctic–Indian migrant, Emberiza bruniceps

Migration is a seasonal phenomenon, wherein the birds swap between their breeding and overwintering grounds to avoid harsh climatic conditions and maximally utilize the geographical resources available. The annual cycle of a migratory bird broadly comprises non-breeding and breeding phases. The non-breeding phase corresponds to non-migratory life history state (LHS), whereas the breeding phase can be bifurcated into migratory (spring/autumn migration) and reproductive stages. Since most of the migratory birds are nocturnal migrants, this results either in shift or compromised sleep in these organisms for the sake of their reproduction and survival. Thus, an obvious question arises regarding the prevalence and distribution of sleep in these night migrants. Therefore, the present study focuses on the life history state-dependent as well as daily (with reference to night) differences in sleep behavior with special mention of different sleep postures in a migratory bunting, Emberiza bruniceps. For this purpose, male redheaded buntings were procured from the wild, and after acclimation in laboratory condition, were subjected to short (8L:16D) and long (13L:11D) photoperiodic schedules. Short photoperiod corresponds to non-migratory, whereas long photoperiod leads to pre-migratory and migratory LHSs. The results reveal that sleep behavior varied with different life history states of the bird. Non-migratory and pre-migratory states were dominated by front and back sleep postures, whereas migratory phase was dominated by active wakefulness. Not only life history state, even the night itself showed gradation in occurrence of different sleep behaviors. As the study was conducted in different phases of night, phasic distribution of different sleep behaviors was also observed. Thus, the bird under study, redheaded bunting, clearly demonstrated life history state, as well as daily differences in distribution of different sleep behaviors.

Metaphor as a dynamic complex emergence an analysis of the discourse of violence victims

Metaphor is here approached as a complex emergence which results from many internal and external factors such as those of a bio-psychological nature among others. Based on an embodied view which assumes that cognition results from "structural couplings that bring forth a world" (VARELA; THOMPSON; ROSCH,1993); it is assumed that socio-culturally shared beliefs, values and attitudes, individuals' life history, their affective and psychological states, besides embodied factors interact dynamically to cause metaphor emergencies to occur. Such metaphors might incorporate verbal language, gestures, body language etc. Having this view of metaphor as a basis, data gathered from three focal groups composed by volunteer violence victims are analysed. Findings from participants’ talks about ways they cope with the threat posed by urban violence, point to the emergence of several systematic metaphors. VIOLENCE IN FOOTBALL IS A REPELLING FORCE and UNDERSTANDING DIFFERENT SOCIAL GROUPS IS SEEING THEM are the two systematic metaphors analysed here.

Multilocus phylogeny of Acrospermaceae: New epibiotic species and placement of Gonatophragmium, Pseudovirgaria, and Phaeodactylium anamorphs

ABSTRACTAcrospermum is a poorly known genus of epibiotic and saprophytic species with a subcosmopolitan distribution. Here, we investigate the intriguing relationship between Acrospermum and its host plants in the fern family Polypodiaceae, where it occurs upon approximately 45 neotropical species. We conducted phylogenetic analyses using an eight-marker comprehensive ascomycete data set comprising 719 species representing all major lineages along with 23 new Acrospermum specimens sampled from ferns. We ask whether fern-dwelling Acrospermum are monophyletic, whether epibiotic Acrospermum have evolved independently from saprophytic ancestors, and identify anamorphic phases by incorporating sequences for all suspected taxa. Our results corroborate the placement of Acrospermales within the Dothideomycetes with strong support. However, the order remains incertae sedis due to weak support along the branches subtending the clade that includes the Acrospermales plus Dyfrolomycetales. Our results show a strong phylogenetic pattern in lifestyles but do not clearly identify an ancestral life history state. The first divergence in Acrospermaceae splits fungicolous taxa from taxa that inhabit plants; saprophytes and anamorphic phases found on angiosperms occur in both clades. Fungicolous species are monophyletic, whereas species with an epibiotic or necrotic life history upon plants are nonmonophyletic due to the position of the saprophyte A. longisporium. Previously, all Acrospermum collected from ferns were identified as A. maxonii. Our results indicate that this is not monophyletic due to the inclusion of Gonatophragmium triuniae. Two species are described herein as A. gorditum, sp. nov., and A. leucocephalum, sp. nov. We find no instances of co-cladogenesis; however, our ability to detect this is limited by the lack of resolution in the A. maxonii clade. Rather, we see that that the distribution of epibiotic Acrospermum is explained by the overlap between the ecological niche of the Acrospermum species and its host.

Temporal expression of genes coding for aryl-alkamine-N-acetyltransferase and melatonin receptors in circadian clock tissues: Circadian rhythm dependent role of melatonin in seasonal responses

We investigated at the transcriptional level the role of daily rhythm in melatonin secretion in seasonal responses in the migratory blackheaded bunting (Emberiza melanocephala), which when exposed to short (SP) and long (LP) photoperiods exhibits distinct seasonal life-history states (LHSs). We reproduced the seasonal LHS by subjecting buntings to SP (8 h light: 16 h darkness, 8 L:16D), which maintained the nonmigratory/ nonbreeding phenotype, and to LP (16 L:8D), which induced the premigratory/ prebreeding, migratory/ breeding and nonmigratory/ postbreeding phenotypes. Plasma melatonin measured at 4 h intervals showed loss of the daily rhythm in the LP-induced premigratory/ prebreeding and migratory/ breeding LHSs. Subsequently, mRNA expression of genes coding for the aryl-alkamine-N-acetyltransferase (AANAT; the rate-liming enzyme of melatonin biosynthesis) and for the receptors for melatonin (Mel1A, Mel1B and Mel1C) was examined in the retina, pineal and hypothalamus; the interacting independent circadian clocks comprising the songbird circadian timing system. Except AANAT that was not amplified in the hypothalamus, we found significant alterations in both, the level and persistence of 24 h rhythm in mRNA expression of all genes, albeit with photoperiod and seasonal differences between three circadian clock tissues. Particularly, 24 h mRNA expression pattern of all genes, except retinal Mel1A, lacked a significant daily rhythm in the LP-induced migratory/ breeding LHS. These results underscore the overall importance of the circadian rhythm in the role of melatonin in photoperiodically-controlled seasonal responses in migratory songbirds.

Transcriptome-wide changes in testes reveal molecular differences in photoperiod-induced seasonal reproductive life-history states in migratory songbirds.

We investigated the molecular basis of seasonal testicular states in black-headed buntings (Emberiza melanocephala), in which seasonal migrations limit reproduction to a narrow time-window during the year. We examined testicular gene expressions in buntings during short day-induced photosensitive nonreproductive state (SDSE), and during long day-induced early (LDES) and late (LDLS) gonadal maturation and regressed photorefractory (LDRF) seasonal states. Using Kallisto, we pseudoaligned the RNA-Seq transcripts and calculated the transcript abundance. We found 1,799 differentially expressed genes (DEGs) between the four photoperiod-induced seasonal states. Further pairwise comparison with SDSE revealed 1,187, 1,224, and 1,238 DEGs in LDES, LDLS, and LDRF, respectively; 852 genes were common to three comparisons. We then identified genetic pathways putatively involved in seasonal testicular cycle. DEGs that enriched calcium ion binding were highly expressed in testicular maturation states. Similarly, DEGs that enriched glycolytic pathway were highly expressed in LDES and LDRF states. More specifically, quantitative polymerase chain reaction showed significant differences between the photoperiod-induced states in testicular expression of genes (HOOK1, RGS2, PRDX4, BCL6, CYFIP2, PDCD4, P2RX4, and GABRA1) involved in gametogenesis and associated pathways. Overall, these results show significant transcriptional differences, and provide insights into the molecular basis of seasonal changes in the reproductive life-history states in a photoperiodic species.

Making use of multiple surveys: Estimating breeding probability using a multievent-robust design capture-recapture model.

Increased environmental stochasticity due to climate change will intensify temporal variance in the life‐history traits, and especially breeding probabilities, of long‐lived iteroparous species. These changes may decrease individual fitness and population viability and is therefore important to monitor. In wild animal populations with imperfect individual detection, breeding probabilities are best estimated using capture–recapture methods. However, in many vertebrate species (e.g., amphibians, turtles, seabirds), nonbreeders are unobservable because they are not tied to a territory or breeding location. Although unobservable states can be used to model temporary emigration of nonbreeders, there are disadvantages to having unobservable states in capture–recapture models. The best solution to deal with unobservable life‐history states is therefore to eliminate them altogether. Here, we achieve this objective by fitting novel multievent‐robust design models which utilize information obtained from multiple surveys conducted throughout the year. We use this approach to estimate annual breeding probabilities of capital breeding female elephant seals (Mirounga leonina). Conceptually, our approach parallels a multistate version of the Barker/robust design in that it combines robust design capture data collected during discrete breeding seasons with observations made at other times of the year. A substantial advantage of our approach is that the nonbreeder state became “observable” when multiple data sources were analyzed together. This allowed us to test for the existence of state‐dependent survival (with some support found for lower survival in breeders compared to nonbreeders), and to estimate annual breeding transitions to and from the nonbreeder state with greater precision (where current breeders tended to have higher future breeding probabilities than nonbreeders). We used program E‐SURGE (2.1.2) to fit the multievent‐robust design models, with uncertainty in breeding state assignment (breeder, nonbreeder) being incorporated via a hidden Markov process. This flexible modeling approach can easily be adapted to suit sampling designs from numerous species which may be encountered during and outside of discrete breeding seasons.