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Novel genetic association with migratory diapause in Australian monarch butterflies.

BACKGROUND: Monarch butterflies (Danaus plexippus) are a charismatic and culturally important North American butterfly species famous for their unique, dramatic migratory life history. While non-migratory populations of the species are widespread and apparently stable, migratory populations in North America have recently seen declines, prompting concern that the migratory phenomenon in North America may be at risk of disappearing. In contrast, a relatively recently-established monarch population in Australia has rapidly re-acquired a migratory life history following hundreds of generations of residency and successive bottlenecks as the species island-hopped across the Pacific during the late 1800s and early 1900s. The process by which migration re-emerged in Australian monarchs is not currently known. RESULTS: We raised and sequenced individuals from Queensland, Australia under environmental conditions associated with migration initiation and found strong variance in reproductive diapause, a key migratory trait, between families which was associated with variation at the spectrin beta chain protein Karst. This protein is known to be involved in diapause termination in monarchs but has not previously been identified as associated with migratory life history variance. The most strongly associated migratory SNPs are also present at a low frequency in North America, suggesting that the Australian population is leveraging standing variation which persisted across repeated bottlenecks as Monarchs spread across the Pacific. CONCLUSIONS: Our results provide an intriguing example of how the temporary loss of migration-in this case likely over hundreds of generations-may not entail the loss of genetic variation associated with this complex life history strategy.

Animals

Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies.

Range expansions can result in founder effects, increasing genetic differentiation between expanding populations and reducing genetic diversity along the expansion front. However, few studies have addressed these effects in long-distance migratory species, for which high dispersal ability might counter the effects of genetic drift. Monarchs (Danaus plexippus) are best known for undertaking a long-distance annual migration in North America, but have also dispersed around the world to form populations that do not migrate or travel only short distances. Here, we used microsatellite markers to assess genetic differentiation among 18 monarch populations and to determine worldwide colonization routes. Our results indicate that North American monarch populations connected by land show limited differentiation, probably because of the monarch's ability to migrate long distances. Conversely, we found high genetic differentiation between populations separated by large bodies of water. Moreover, we show evidence for serial founder effects across the Pacific, suggesting stepwise dispersal from a North American origin. These findings demonstrate that genetic drift played a major role in shaping allele frequencies and created genetic differentiation among newly formed populations. Thus, range expansion can give rise to genetic differentiation and declines in genetic diversity, even in highly mobile species.

Animal Distribution

Amino Acid Substitutions in the Na+/K+-ATPase May Contribute to Salinity Tolerance in Insects.

Environmental salinity levels vary naturally across terrestrial ecosystems but can be heightened locally by coastal proximity and desertification as well as human activities such as road salt application and agriculture. Since salt is essential for many physiological processes in insects, rising environmental sodium concentrations may drive behavioral changes, where insects select environments and food sources with suitable sodium levels, or evolutionary changes in constitutive or plastic physiological mechanisms to process salt, potentially altering ecological dynamics and species interactions.Numerous hematophagous (blood feeding) insects such as the yellow-fever mosquito Aedes aeqypti are known to be able to breed in relatively saline environments. Among phytophagous (plant feeding) insects, grasshoppers can be important herbivores in arid and coastal salt-affected regions, whereas the monarch butterfly (Danaus plexippus) appears to perform relatively well on milkweed host plants growing in roadsides influenced by salt runoff. Several of these insects share a common trait: amino acid substitutions in the first extracellular loop of the Na+/K+-ATPase (NKA), a sodium pump crucial for maintaining ion balance. For the monarch these substitutions confer resistance to toxic cardenolides from milkweeds, but it is unclear whether NKA substitutions may influence salt tolerance.Here, we investigate whether the NKA substitutions found in these insects may contribute to salt tolerance using gene-edited Drosophila melanogaster mutant strains as models. We show that flies with substitution Q111L (found in Aedes mosquitoes) or a combination of Q111L and A119S (found in grasshoppers) exhibited greater salt tolerance, whereas flies carrying the combination of substitutions found in the monarch (Q111V, A119S, and N122H) did not.Our results suggest that the monarch may rely on alternate mechanisms for salt tolerance and that its NKA substitutions are important primarily for cardenolide resistance. However, substitution Q111L and the combination of Q111L and A119S may be relevant for salt tolerance in a variety of insects. Uncovering mechanisms of salt tolerance enhances our understanding of species distributions, ecological interactions, and evolutionary physiology in response to changing environmental salinity levels.

Journal Article