Powell Lab at Binghamton University
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Life history timing and the origin and maintenance of biodiversity

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Phenology, or seasonal timing, is a critical component of adaptation for organisms in temperate environments. From subtropical forests to the arctic tundra, animals, plants, and microbes are challenged by shifting conditions throughout the year. Abiotic conditions such as temperature and precipitation along with seasonal changes in biotic factors, such as the presence or abundance of prey, mutualists, competitors, or parasites may restrict an organism’s ability to thrive throughout the year. We expect natural selection to act strongly on traits that allow organisms to mitigate these seasonal challenges, by allowing them to weather unfavorable conditions and synchronize key life stages – like growth and reproduction, with the right temporal windows.

The evolution of seasonal timing is an important facet of my lab’s dual central questions of ‘how does new biodiversity come about?’ and ‘how is biological variation maintained in the face of environmental change?’.  For the first part, because reproduction is often highly seasonal, phenological adaptation may be a potent driver of speciation. If adaptation to a new ecological opportunity involves a shift in life cycle timing, the resulting offset in mating seasons can rapidly drive reproductive isolation – placing populations on separate evolutionary trajectories on the path to become separate species. Seasonality may therefore be a critical axis of diversification for some groups of organisms, with diversity in seasonal niches setting the stage for temporal adaptive radiations.

For the second question, altered phenology is expected to be one of (if not the) most important ecological ramifications of climate change. For many organisms, particularly ectotherms like insects, the direct effects of increased temperatures in the coming decades may not pose existential threats to populations, in terms of being able to survive and grow in slightly warmer conditions. However, the changing climate may have drastic effects on the environmental cues that organisms use to maintain adaptive life cycle timing. An increase in a few degrees across seasons, shortened winters, or increased variability during seasonal transitions may pull the phenological rug out from under ecological communities, driving maladaptive life history responses or decoupling seasonal synchrony across closely interacting organisms.

Much of the work in my lab focuses on understanding the ecological and genomic factors that promote or constrain rapid adaptation to novel seasonal conditions. We are interested in questions such as the eco-physiological basis of variation in life history timing, how standing genetic variation underlying seasonal adaptation is maintained in populations, the genomic architecture of dormancy traits, the role of phenological divergence in adaptive radiations, and predicting how populations and communities will respond to future seasonal regimes. These questions of seasonal adaptation are relevant to all of the study systems our groups works with, including seed dispersing ants and gall-former/parasitoid communities (see below), but this forms the basis of our primary work with Rhagoletis flies: a model system for both ecological speciation-in-action and rapid phenological adaptation.
















Rhagoletis pomonella is a specialist Tephritid fruit fly that ancestrally infested the fruit of hawthorn trees in eastern North America. In the 1850s, a population of these flies shifted to specializing on infesting apples - which had been introduced by European colonizers two centuries earlier. Shifting to this novel host required adaptation in two key traits: 1) chemosensory behavioral adaptation shaping attraction and avoidance to the fruit surface volatiles used by the flies to find mating and oviposition sites and 2) dormancy-mediated life history timing, synchronizing the short-lived adult life stage with the brief period of available ripe host fruit, which occurs 3-4 weeks earlier for apple compared to hawthorn. Both ecological traits play a direct role in the flies' system of mating, driving both prezygotic and postzygotic reproductive isolation. Gene  flow between apple and hawthorn flies in places where the trees grow side-by-side is limited to ~4% per generation, placing these flies in an intermdiate phase of the speciaiton process in just the past ~160 years.

This evolutionary shift to an earlier life cycle timing during recent historical times is closely analagous to what we expect many populations may be faced with in the coming decades under climate change. Our work includes both further elucidating the classic speciation story in Rhagoletis and also developing this as a powerful system for studying rapid adaptation to climate change. Current projects include:  testing for phenotypic and genomic responses to simulated climate change using environmental chambers that mimic natural soil temperature conditions for R. pomonella pupae, determining how genetic variation underlying seasonal adaptation is maintained within and across populations, investigating how different facets of climate change - such as shortened winters and increased volatility in winter/spring transitions may disrupt adaptive life history timing, and integrating phenotypic and population genomic data at broad geographic scales to predict thresholds of vulnerability  to altered seasonal regimes across populations.


How ecologically important variation builds up along the speciation continuum

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Understanding how functional ecological variation is partiaiotned in nature is an improant goal in ecology. Traditionally, the functional importance of biodiversity has been assessed at the level of species… are species interchangeable in their ecological roles, and does increased species diversity lead to increased ecosystem function or resiliency? However, there is now a growing appreciation of the importance of intraspecific variation in driving ecological outcomes as well. These two levels of biodiversity, intra- and interspecific, do not represent discrete levels of biological organization, as the process of speciation may often produce a continuous gradient between divergently selected variation segregating within populations to fully isolated species on independent evolutionary trajectories. Thus, cases of incomplete speciation, where populations straddle some range of the “speciation continuum” may allow us to ask questions about howa and when nascent differences between diverging populations begin to matter in ecosystems.

My lab has been addressing these questions through a long-term collaboration with the Prior lab at BU, investigating speciation and ecosystem outcomes in a species complex of ants that act as keystone seed-dispersing mutualists in Northeastern deciduous forests. Specialized seed dispersal by ants, or myrmecochory, is a common and important mutualism in many temperate environments, involving >10,000 species of plants worldwide. The northeastern forests of North America are considered a hotbed of this interaction, with many familiar wildflowers like trillium and violets producing specialized lipid-rich appendages called elaisomes on their seeds to entice ants to carry them away from the parent plant and eventually deposit them in the favorable conditions of ant colony refuse. While many ant species engage in this behavior, myrmecochory in this region is dominated by a species complex of ants in the genus Aphaenogaster
. In some areas, >75% of dispersal events are driven by ants in this group. The seed dispersing Aphaenogaster ants do not all segregate neatly into discrete species. Some like A. fulva appear to be both reciprocally monophyletic from the rest of the group and morphologically distinguishable, while others, particularly the nominal species A. picea and A. rudis have proven notoriously difficult to resolve. Evidence our group has collected, such as intermediate phenotypes occurring at sympatric sites, points to this ambiguity being driven by these taxa being in an incomplete portion of the speciation continuum… either in the midst of ongoing divergence or experiencing hybridization following secondary contact.

We are using population genomic and morphometric approaches to understand patterns of genetic and phenotypic diversity across this species complex and collaborating with the Prior lab on behavioral assays and field experiments to test how genetic diversity within this complex scales up to ecologically relevant diversity, with differences in foraging behavior, seed preference, colongy phenology, and thermal tolerances potentially scaling up to effect the structure of understory plant communities.

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Tritrophic adaptation and speciation in specialist insect-parasitoid systems

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Speciation does not occur in an ecological vacuum. As with the seed dispersing ant complex above, the diversity shaped by on-going speciation can ripple out into the broader community. Another major focus of the lab is understanding the complex coevolutionary feedbacks that may arise as ecological divergence leads to altered species interactions. We are interested in how diversity may beget diversity as ecological speciation at lower trophic levels may open novel niches for higher trophic levels to divergently adapt to in turn - a phenomenon that has been well documented in the parasitoid community surrounding
Rhagoletis flies. However, this may not always be a one-way street, as interactions with parasitoids and predators may play an important role in shaping the divergent fitness landscapes posed by host plants.

The lab is currently addressing these questions in Rhagoletis  as well as systems of  gall-forming insects. Gall-formers have particularly intimate coevolutionary relationships with their host plants -- highjacking the plant's gene regulatory system to build specialized plant structures to house and feed the insects. The tremendous diversity of gall shapes, sizes, and plant tissue types may be driven in part by their role in protecting their inhabitants from parasitoid attack. Thus, differences in parasitoid interactions across host plants may form an axis of divergent selection for gall-formers, shaping the Gene x Gene x Environment interactions influencing gall development. 

We are examining these questions using the goldenrod gall fly, Eurosta solidaginis, which is divergently adapted to two closely related host plants, Solidago altissima and Solidago gigantea in the Northeast and it's community of parasitoid wasps and beetles. This system also shares a strong seasonal adaptation component with Rhagoletis, with diapause-mediated adult eclosion phenology being an important part of the story. Current projects include the population genomics of divergence across trophic levels and testing how parasitoids alter natural selection on gall size between Eurosta population infesting both host plants at sympatric sites.

In addition, we are asking similar questions about the evolutionary ecology of gall-parasitoid interactions in far more diverse system of oak gall wasps in the Pacific Northwest. In a long-term collaboration with the Prior lab at BU, funded in part by a grant from the National Geographic Society, we are interested in how these interactions may evolve across range-expansion fronts.



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