Adam M. Fudickar

Seasonal timing and population divergence: when to breed, when to migrate

Understanding how populations adapt to constantly changing environments requires approaches drawn from integrative and evolutionary biology as well as population ecology. Timing of reproduction and migration reflect seasonal pulses in resources, are driven by day length, and are also responsive to environmental cues that change with climate. Researchers focusing on birds have discovered accelerated breeding, reductions in migration, and extensive variation in perception, transduction, and response to the environment. We consider situations in which individuals experience the same environment but differ in the timing of the annual cycle. Such scenarios provide exceptional opportunities to study mechanisms related to among-population differences in timing (allochrony) and distribution (sympatry–allopatry–heteropatry), which have the potential either to enhance or reduce population divergence and biodiversity.

Reproductive Allochrony in Seasonally Sympatric Populations Maintained by Differential Response to Photoperiod: Implications for Population Divergence and Response to Climate Change.

Reproductive allochrony presents a potential barrier to gene flow and is common in seasonally sympatric migratory and sedentary birds. Mechanisms mediating reproductive allochrony can influence population divergence and the capacity of populations to respond to environmental change. We asked whether reproductive allochrony in seasonally sympatric birds results from a difference in response to supplementary or photoperiodic cues and whether the response varies in relation to the distance separating breeding and wintering locations as measured by stable isotopes. We held seasonally sympatric migratory and sedentary male dark-eyed juncos (Junco hyemalis) in a common garden in early spring under simulated natural changes in photoperiod and made measurements of reproductive and migratory physiology. On the same dates and photoperiods, sedentary juncos had higher testosterone (initial and gonadotropin-releasing hormone induced), more developed cloacal protuberances, and larger testes than migrants. In contrast, migratory juncos had larger fat reserves (fuel for migration). We found a negative relationship between testis mass and feather hydrogen isotope ratios, indicating that testis growth was more delayed in migrants making longer migrations. We conclude that reproductive allochrony in seasonally sympatric migratory and sedentary birds can result from a differential response to photoperiodic cues in a common garden, and as a result, gene flow between migrants and residents may be reduced by photoperiodic control of reproductive development. Further, earlier breeding in response to future climate change may currently be constrained by differential response to photoperiodic cues.

Differential gene expression in seasonal sympatry: mechanisms involved in diverging life histories.

In an era of climate change, understanding the genetic and physiological mechanisms underlying flexibility in phenology and life history has gained greater importance. These mechanisms can be elucidated by comparing closely related populations that differ in key behavioural and physiological traits such as migration and timing of reproduction. We compared gene expression in two recently diverged dark-eyed Junco ( Junco hyemalis) subspecies that live in seasonal sympatry during winter and early spring, but that differ in behaviour and physiology, despite exposure to identical environmental cues. We identified 547 genes differentially expressed in blood and pectoral muscle. Genes involved in lipid transport and metabolism were highly expressed in migrant juncos, while genes involved in reproductive processes were highly expressed in resident breeders. Seasonal differences in gene expression in closely related populations residing in the same environment provide significant insights into mechanisms underlying variation in phenology and life history, and have potential implications for the role of seasonal timing differences in gene flow and reproductive isolation.

Early spring sex differences in luteinizing hormone response to gonadotropin releasing hormone in co-occurring resident and migrant dark-eyed juncos (Junco hyemalis)

Highlights • In early spring female juncos vary in LH following repeated stimulation with GnRH.• Resident and migrant males do not vary in LH.• Suggests the pituitary as a critical point of control for reproductive timing.• Sex difference suggests selection shaped responsiveness at critical time points.

Understanding variation in migratory movements: A mechanistic approach

Spatial and temporal fluctuations in resource availability have led to the evolution of varied migration patterns. In order to appropriately time movements in relation to resources, environmental cues are used to provide proximate information for timing and the endocrine system serves to integrate these external cues and behavioral and physiological responses. Yet, the regulatory mechanisms underlying migratory timing have rarely been compared across a broad range of migratory patterns. First, we offer an updated nomenclature of migration using a mechanistic perspective to clarify terminology describing migratory types in relation to ecology, behavior and endocrinology. We divide migratory patterns into three types: obligate, nomadic, and fugitive. Obligate migration is characterized by regular and directed annual movements between locations, most commonly for breeding and overwintering, where resources are predictable and sufficient. Nomadic migrations occur less predictably than do obligate migrations as animals make use of potentially rich but ephemeral resources that occur unpredictably in space or time. Fugitive migrations move animals away from an area in response to severe disruption of environmental conditions and occur as part of an emergency life history stage. We also consider partially migratory populations, which include a mix of sedentary and migratory individuals; the movement patterns of partial migrants are expected to fall into one of the three types above. For these various forms of migration, we review our understanding of the environmental cues and endocrine mechanisms that underlie the expression of a migratory state. Several common hormonal mechanisms exist across the varied migratory forms, but there are also important areas where further investigations are needed in order to gain broad insight into the origin of movements and the diversity of migratory patterns. We propose that taking a comparative approach across the migratory types that considers endocrine mechanisms will advance a new understanding of migration biology.

Mechanisms associated with an advance in the timing of seasonal reproduction in an urban songbird

The colonization of urban environments by animals is often accompanied by earlier breeding and associated changes in seasonal schedules. Accelerated timing of seasonal reproduction in derived urban populations is a potential cause of evolutionary divergence from ancestral populations if differences in physiological processes that regulate reproductive timing become fixed over time. We compared reproductive development in free-living and captive male dark-eyed juncos deriving from a population that recently colonized a city (~35 years) and ceased migrating to that of conspecifics that live in sympatry with the urban population during winter and spring but migrate elsewhere to breed. We predicted that the earlier breeding sedentary urban birds would exhibit accelerated reproductive development along the hypothalamic-pituitary (HPG) axis as compared to migrants. We found that free-living sedentary urban and migrant juncos differed at the level of the pituitary when measured as baseline luteinizing hormone (LH) levels, but not in increased LH when challenged with Gonadotropin-Releasing Hormone (GnRH). Among captives held in a common garden, and at the level of the gonad, we found that sedentary urban birds produced more testosterone in response to GnRH than migrants living in the same common environment, suggesting greater gonadal sensitivity in the derived urban population. Greater gonadal sensitivity could arise from greater upstream activation by LH or FSH or from reduced suppression of gonadal development by the adrenal axis. We compared abundance of gonadal transcripts for LH receptor (LHR), follicle stimulating hormone receptor (FSHR), glucocorticoid receptor (GR), and mineralocorticoid receptor (MR) in the common-garden, predicting either more abundant transcripts for LHR and FSHR or fewer transcripts for GR and MR in the earlier breeding sedentary urban breeders, as compared to the migrants. We found no difference in the expression of these genes. Together the data suggest that advanced timing of reproduction in a recently derived urban population is facilitated by earlier increase in upstream baseline activity of the HPG and earlier release from gonadal suppression by yet-to-be-discovered mechanisms. Evolutionarily, our results suggest that potential for gene flow between seasonally sympatric populations may be limited due to urban-induced advances in the timing of reproduction and resulting allochrony

Genomes to space stations: the need for the integrative study of migration for avian conservation

Ongoing changes to global weather patterns and human modifications of the environment have altered the breeding and non-breeding ranges of migratory species, the timing of their migrations, and even whether they continue to migrate at all. Animal movements are arguably one of the most difficult behaviours to study, particularly in smaller birds that migrate tens to thousands of kilometres seasonally, often moving hundreds of kilometres each day. The recent miniaturization of tracking and logging devices has led to a radical transformation in our understanding of avian migratory behaviour and migratory connectivity. While advances in technology have altered the way researchers study migratory behaviour in the field, advances in techniques related to the study of physiological and genetic mechanisms underlying migratory behaviour have rarely been integrated into field studies of tracking. To predict the capacity of migrants to adjust to a changing planet, it is essential that we combine avian migration data with physiological and genetic measurements taken at key time points prior to, during and after migration.

Migration confers winter survival benefits in a partially migratory songbird

To evolve and to be maintained, seasonal migration, despite its risks, has to yield fitness benefits compared with year-round residency. Empirical data supporting this prediction have remained elusive in the bird literature. To test fitness related benefits of migration, we studied a partial migratory population of European blackbirds (Turdus merula) over 7 years. Using a combination of capture-mark-recapture and radio telemetry, we compared survival probabilities between migrants and residents estimated by multi-event survival models, showing that migrant blackbirds had 16% higher probability to survive the winter compared to residents. A subsequent modelling exercise revealed that residents should have 61.25% higher breeding success than migrants, to outweigh the survival costs of residency. Our results support theoretical models that migration should confer survival benefits to evolve, and thus provide empirical evidence to understand the evolution and maintenance of migration.

Seasonally sympatric but allochronic: differential expression of hypothalamic genes in a songbird during gonadal development

Allochrony, the mismatch of reproductive schedules, is one mechanism that can mediate sympatric speciation and diversification. In songbirds, the transition into breeding condition and gonadal growth is regulated by the hypothalamic–pituitary–gonadal (HPG) axis at multiple levels. We investigated whether the difference in reproductive timing between two seasonally sympatric subspecies of dark-eyed juncos (Junco hyemalis) was related to gene expression along the HPG axis. During the sympatric pre-breeding stage, we measured hypothalamic and testicular mRNA expression of candidate genes via qPCR in captive male juncos. For hypothalamic mRNA, we found our earlier breeding subspecies had increased expression of gonadotropin-releasing hormone (GnRH) and decreased expression of androgen receptor, oestrogen receptor alpha and mineralocorticoid receptor (MR). Subspecies did not differ in expression of hypothalamic gonadotropin-inhibitory hormone (GnIH) and glucocorticoid receptor (GR). While our earlier breeding subspecies had higher mRNA expression of testicular GR, subspecies did not differ in testicular luteinizing hormone receptor, follicle-stimulating hormone receptor or MR mRNA expression levels. Our findings indicate increased GnRH production and decreased hypothalamic sensitivity to sex steroid negative feedback as factors promoting differences in the timing of gonadal recrudescence between recently diverged populations. Differential gene expression along the HPG axis may facilitate species diversification under seasonal sympatry.

Data from: Sedentary songbirds maintain higher prevalence of haemosporidian parasite infections than migratory conspecifics during seasonal sympatry

Long-distance migrations influence the physiology, behavior, and fitness of migratory animals throughout their annual cycles, and fundamentally alter their interactions with parasites. Several hypotheses relating migratory behavior to the likelihood of parasitism have entered the literature, making conflicting, testable predictions. To assess how migratory behavior of hosts is associated with parasitism, we compared haemosporidian parasite infections between two closely related populations of a common North American sparrow, the dark-eyed junco, that co-occur in shared habitats during the non-breeding season. One population is sedentary and winters and breeds in the Appalachian Mountains. The other population is migratory and is found in seasonal sympatry with the sedentary population from October through April, but then flies (≥ 900 km) northwards to breed. The populations were sampled in the wild on the shared montane habitat at the beginning of winter and again after confining them in a captive common environment until the spring. We found significantly higher prevalence of haemosporidian parasite infections in the sedentary population. Among infected juncos, we found no difference in parasite densities (parasitemias) between the sedentary and migrant populations and no evidence for winter dormancy of the parasites. Our results suggest that long-distance migration may reduce the prevalence of parasite infections at the population level. Our results are inconsistent with the migratory exposure hypothesis, which posits that long-distance migration increases exposure of hosts to diverse parasites, and with the migratory susceptibility hypothesis, which posits that trade-offs between immune function and migration increase host susceptibility to parasites. However, our results are consistent with the migratory culling hypothesis, which posits that heavily infected animals are less likely to survive long-distance migration, and with the migratory escape hypothesis, which posits that long-distance migration allows host populations to seasonally escape areas of high infection risk.