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1. Population genetics of a recent range expansion and subsequent loss of migration in monarch butterflies

   https://doi.org/10.1111/mec.16592  

   Hemstrom, William B. ; Freedman, Micah G. ; Zalucki, Myron P. ; Ramírez, Santiago R. ; Miller, Michael R. ( July 2022 , Molecular Ecology)

   Range expansions—whether permanent or transient—strongly influence the distribution of genetic variation in space. Monarch butterflies are best known for long‐distance seasonal migration within North America but are also established as nonmigratory populations around the world, including on Pacific Islands. Previous research has highlighted stepwise expansion across the Pacific, though questions remain about expansion timing and the population genetic consequences of migration loss. Here, we present reduced‐representation sequencing data for 275 monarchs from North America (n = 85), 12 Pacific Islands (n = 136) and three locations in Australia (n = 54), with the goal of understanding (i) how the monarch's Pacific expansion has shaped patterns of population genetic variation and (ii) how loss of migration has influenced spatial patterns of differentiation. We find support for previously described stepwise dispersal across the Pacific and document an additional expansion from Hawaii into the Mariana Islands. Nonmigratory monarchs within the Mariana Islands show strong patterns of differentiation, despite their proximity; by contrast, migratory North American samples form a single genetically panmictic population across the continent. Estimates of Pacific establishment timing are highly uncertain (~100–1,000,000 years ago) but overlap with historical records that indicate a recent expansion. Our data support (i) a recent expansion across the Pacific whose timing overlaps with available historical records of establishment and (ii) a strong role for seasonal migration in determining patterns of spatial genetic variation. Our results are noteworthy because they demonstrate how the evolution of partial migration can drive population differentiation over contemporary timescales.

    

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2. Seasonal plasticity in morphology and metabolism differs between migratory North American and resident Costa Rican monarch butterflies

   https://doi.org/10.1002/ece3.9796  

   Tenger‐Trolander, Ayşe ; Julick, Cole R. ; Lu, Wei ; Green, Delbert André ; Montooth, Kristi L. ; Kronforst, Marcus R. ( February 2023 , Ecology and Evolution)

   Environmental heterogeneity in temperate latitudes is expected to maintain seasonally plastic life‐history strategies that include the tuning of morphologies and metabolism that support overwintering. For species that have expanded their ranges into tropical latitudes, it is unclear the extent to which the capacity for plasticity will be maintained or will erode with disuse. The migratory generations of the North American (NA) monarch butterflyDanaus plexippuslead distinctly different lives from their summer generation NA parents and their tropical descendants living in Costa Rica (CR). NA migratory monarchs postpone reproduction, travel thousands of kilometers south to overwinter in Mexico, and subsist on little food for months. Whether recently dispersed populations of monarchs such as those in Costa Rica, which are no longer subject to selection imposed by migration, retain ancestral seasonal plasticity is unclear. To investigate the differences in seasonal plasticity, we reared the NA and CR monarchs in summer and autumn in Illinois, USA, and measured the seasonal reaction norms for aspects of morphology and metabolism related to flight. NA monarchs were seasonally plastic in forewing and thorax size, increasing wing area and thorax to body mass ratio in autumn. While CR monarchs increased thorax mass in autumn, they did not increase the area of the forewing. NA monarchs maintained similar resting and maximal flight metabolic rates across seasons. However, CR monarchs had elevated metabolic rates in autumn. Our findings suggest that the recent expansion of monarchs into habitats that support year‐round breeding may be accompanied by (1) the loss of some aspects of morphological plasticity as well as (2) the underlying physiological mechanisms that maintain metabolic homeostasis in the face of temperature heterogeneity.

    

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3. Elevated atmospheric concentrations of CO 2 increase endogenous immune function in a specialist herbivore

   https://doi.org/10.1111/1365-2656.13395  

   Decker, Leslie E. ; Jeffrey, Christopher S. ; Ochsenrider, Kaitlin M. ; Potts, Abigail S. ; de Roode, Jacobus C. ; Smilanich, Angela M. ; Hunter, Mark D. ; Ardia, ed., Daniel ( December 2020 , Journal of Animal Ecology)

   Animals rely on a balance of endogenous and exogenous sources of immunity to mitigate parasite attack. Understanding how environmental context affects that balance is increasingly urgent under rapid environmental change. In herbivores, immunity is determined, in part, by phytochemistry which is plastic in response to environmental conditions. Monarch butterfliesDanaus plexippus, consistently experience infection by a virulent parasiteOphryocystis elektroscirrha, and some medicinal milkweed (Asclepias) species, with high concentrations of toxic steroids (cardenolides), provide a potent source of exogenous immunity.

   We investigated plant‐mediated influences of elevated CO₂(eCO₂) on endogenous immune responses of monarch larvae to infection byO. elektroscirrha. Recently, transcriptomics have revealed that infection byO. elektroscirrhadoes not alter monarch immune gene regulation in larvae, corroborating that monarchs rely more on exogenous than endogenous immunity. However, monarchs feeding on medicinal milkweed grown under eCO₂lose tolerance to the parasite, associated with changes in phytochemistry. Whether changes in milkweed phytochemistry induced by eCO₂alter the balance between exogenous and endogenous sources of immunity remains unknown.

   We fed monarchs two species of milkweed;A. curassavica(medicinal) andA. incarnata(non‐medicinal) grown under ambient CO₂(aCO₂) or eCO₂. We then measured endogenous immune responses (phenoloxidase activity, haemocyte concentration and melanization strength), along with foliar chemistry, to assess mechanisms of monarch immunity under future atmospheric conditions.

   The melanization response of late‐instar larvae was reduced on medicinal milkweed in comparison to non‐medicinal milkweed. Moreover, the endogenous immune responses of early‐instar larvae to infection byO. elektroscirrhawere generally lower in larvae reared on foliage from aCO₂plants and higher in larvae reared on foliage from eCO₂plants. When grown under eCO₂, milkweed plants exhibited lower cardenolide concentrations, lower phytochemical diversity and lower nutritional quality (higher C:N ratios). Together, these results suggest that the loss of exogenous immunity from foliage under eCO₂results in increased endogenous immune function.

   Animal populations face multiple threats induced by anthropogenic environmental change. Our results suggest that shifts in the balance between exogenous and endogenous sources of immunity to parasite attack may represent an underappreciated consequence of environmental change.

    

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4. Are eastern and western monarch butterflies distinct populations? A review of evidence for ecological, phenotypic, and genetic differentiation and implications for conservation

   https://doi.org/10.1111/csp2.432  

   Freedman, Micah G. ; de Roode, Jacobus C. ; Forister, Matthew L. ; Kronforst, Marcus R. ; Pierce, Amanda A. ; Schultz, Cheryl B. ; Taylor, Orley R. ; Crone, Elizabeth E. ( May 2021 , Conservation Science and Practice)

   Monarch butterflies are a species of conservation priority due to declining overwintering populations in both eastern and western North America. Declines in western overwintering monarchs—more than 99.9% since monitoring began—are especially acute. However, the degree to which western monarchs are a distinct biological entity is uncertain. In this review, we focus on phenotypic and genetic differentiation between eastern and western monarchs, with the goal of informing researchers and policy‐makers who are interested in monarch conservation. Eastern and western monarchs occupy distinct environments and show some evidence for phenotypic differentiation, particularly for migration‐associated traits, though population genetic and genomic studies suggest that they are indistinguishable from one another. We suggest future studies that could improve our understanding of differences between eastern and western monarchs. We also discuss the concept of adaptive capacity in eastern and western monarchs as well as non‐migratory populations outside of the monarch's primary North American range. Finally, we discuss the prospect of completely losing migratory monarchs from western North America and what this entails for monarch conservation.

    

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5. Monarch butterflies reared under autumn‐like conditions have more efficient flight and lower post‐flight metabolism

   https://doi.org/10.1111/een.12828  

   Schroeder, Hayley ; Majewska, Ania ; Altizer, Sonia ( December 2019 , Ecological Entomology)

   1. Many migratory animals undergo physiological and behavioural changes to prepare for and sustain long‐distance movements. Because insect migrations are common and diverse, studies that examine how migratory insects meet the energetic demands of long‐distance movements are badly needed.

   2. Monarch butterflies (Danaus plexippus) migrate up to 4000 km annually from eastern North America to wintering sites in central Mexico. Autumn generation monarchs undergo physiological and behavioural changes in response to environmental cues to initiate migration. In particular, exposure to cooler temperatures and shorter day lengths in early autumn causes monarchs to enter the hormonally induced state of reproductive diapause.

   3. This study examined differences in flight‐associated metabolic rate (MR) and flight performance metrics for monarchs experimentally reared under autumn‐like conditions (typically experienced before the southward migration) relative to monarchs reared under summer‐like conditions.

   4. Adult monarchs reared under autumn‐like conditions showed lower post‐flight MRs, greater flight efficiency, and lower measures of reproductive activity relative to monarchs reared under summer‐like conditions. Increases in post‐flight metabolism were associated with monarch body weight, age, and flight velocity.

   5. These findings suggest that a trans‐generational shift in flight energetics is an important component of the monarch's complex migratory syndrome, and that physiological changes that accompany reproductive diapause facilitate energy conservation during flight.

    

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