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William E. Bradshaw and Christina M. Holzapfel | |
---|---|
![]() Christina Holzapfel and William Bradshaw collecting disease-bearing mosquitoes in 2015. | |
Born | William: Orange, New Jersey (1942) Christina: Baltimore, Maryland (1942) |
Spouse | William: Christina Holzapfel Christina: William Bradshaw |
Scientific career | |
Fields | Evolutionary biology and genetics |
Institutions | University of Oregon, Imperial College, Tall Timbers Research Station, Harvard University, The University of Michigan, Princeton University |
Website | https://bradshaw-holzapfel-lab.uoregon.edu |
William Bradshaw (1942) and Christina Holzapfel (1942) are an American couple who are evolutionary biologists and geneticists at the University of Oregon. Although the scope of their work has traversed fields as diverse as the physics of light[1] to speciation of endemic plants in the Canary Islands,[2] their startling discovery[3] that recent climate change has penetrated to the level of the gene and is driving evolution in nature in as few as five years[4][5][6][7] awakened the world at large to the urgency of addressing this impending dilemma.[8][9][10][11] In 2007, their lab was distinguished by the National Science Foundation as one of 10 from among all disciplines "that best meets the primary mission of NSF for DISCOVERY, "to foster research that will advance frontiers of knowledge, emphasizing areas of greatest opportunity and potential benefit in establishing the nation as a global leader in fundamental and transformational science and engineering." Their work is memorialized through an NSF OPUS award to support a website, available in perpetuity, illustrating many of their diverse discoveries.
Early Years
editWilliam Emmons Bradshaw was born in Orange, New Jersey in 1942, and was raised on a dairy farm in Bucks County, Pennsylvania, where he learned the value of a solid work ethic and basic carpentry and electrical skills, later of great value to an experimental biologist. He developed an early interest in insects and most anything biological. He attended the Millbrook School, where he explored the surrounding swamps and bogs, sometimes accompanied by fellow Millbrook biology students Thomas Lovejoy and Egbert Leigh. In a nearby bog, he first encountered and was fascinated by carnivorous pitcher plants, unaware of their inhabitants and the role they would play in his future. After Millbrook, he attended Princeton University. He spent one summer working with Glenn Jepsen in the Bighorn Basin of Wyoming on Paleocene and Eocene fossil mammals. In preparation for work in the field, he articulated an entire deer skeleton to learn mammalian osteology – knowledge that stood him in good stead that summer. He completed a year of reading and conference on insect physiology and diapause with Colin Pittendrigh, writing a monograph on systematics and evolution of Peripatus, affirming their intermediate position between annelids and arthropods. Subsequently, he continued experimental research with Pittendrigh for over a year, showing diurnal rhythms of neurosecretion in the dorsal midbrain of Pectinophora, the pink bollworm. He later used his knowledge of histology to exclude the elusive hindgut hormone, "proctodone"[12] as being relevant to diapause in the pink bollworm, convincingly ending subsequent research by Pittendrigh in that direction.
His doctoral research at the University of Michigan with David Shappirio concerned photoperiodism and seasonal development of Chaoborus, a carnivorous midge of shallow fishless ponds. Using Chaoborus, he discovered a unique synergistic interaction between photoperiod and food (prey) for the termination of diapause,[13] determined the first action spectra (building, wiring, and plumbing a toroidal water- and air-cooled apparatus for determining simultaneous sensitivity to 12 wavelengths with variable intensity) for the termination of diapause including both dawn and dusk transitions. From these two action spectra, he was able to determine for the first time, the astronomic units that defined a “day,” regulating seasonal development (photoperiodism) in nature. The comparative dawn and dusk action spectra also showed that Chaoborus, experienced an asymmetric day.[1][14] He also discovered a novel developmental polymorphism between progressive and conservative termination of diapause, maintained by uncertain vernal environments, and ensuring developmental success of at least some of the population in harsh as well as mild spring environments.[15]
At this time, he became a friend of Christina Holzapfel and Kornelius Lems, the three of them sharing an interest in carnivorous plants, swamps, bogs, and classical music. Subsequently, as an NIH post-doctoral Fellow at Harvard, Bill worked with Carroll Williams, determining the effects of Zoëcon ZR515 on non-target aquatic midges (Chironomus). Later, ZR515 was to become the first commercially successful insect hormone analog to be used as a “next-generation” pesticide (Altosid©). While at Harvard, he began a collaboration with Philip Lounibos on the evolution of dormancy in the pitcher-plant mosquito, Wyeomyia smithii, its control by temperature and day length (photoperiodism). They determined for the first time the relationship between altitude and latitude in the evolution of the day length (photoperiod) used by any insect to regulate its seasonal development.[16][17] They also discovered a developmental polymorphism combining both ancestral and derived stages of diapause in northern populations maintained as a, “fail-safe” in uncertain vernal environments,[18] analogous to Chaoborus.[15] These results emphasized the adaptive importance of multiple developmental options when insects are confronted by uncertain seasonal environments.
During this time, Bill continued interaction with Christina Holzapfel, then a post-doctoral Fellow in the Harvard University Gray Herbarium, explaining endemism in diverse species over decades and often millennia.
Christina Marie Holzapfel began her journey as a “farm kid,” born and growing up three miles outside the Baltimore city limit in 1942. The granddaughter of an immigrant violin maker, Carl C. Holzapfel, and daughter of a pioneer school teacher from Cherry Creek Nevada, the themes of her household were God, country, family, and living a purpose-filled life. Everyone worked; generations cared for each other. In the brief free time she was allowed, Chris spent turning over rocks, and wading through the stream that flowed through the family farm, seeking dragonfly larvae, frogs, and salamanders. Among the tangled reeds framing the stream, patches of water-filled leaves of the then strange plants, inhabited by insects, both alive and dead, fascinated Chris. Little did she know that these plants, Sarracenia purpurea, the purple pitcher plant, would later become the focus of her adult life. By the time she entered her large public high school, she was already a Peabody-trained pianist and an illustrator, with the drive to make the world a better place. Having been a 4-H Club member since the age of 10, public speaking and applied skills were familiar to her, and she soon found herself holding class offices, playing varsity sports, and ultimately was elected first the vice president, then President of the Student Government, the first woman to have held these offices in the school's long history. Graduating as “Most Likely to Succeed,” she did her best in the ensuing years to fulfill her classmates’ expectations. An early event in 1960 altered the direction of her life at “Girls’ Nation,” which she attended as “Senior Senator” from Maryland in this annual national conference in Washington, DC. Whereas her male colleagues attending “Boys’ Nation” met with President, Dwight David Eisenhower, and toured the Senate and Oval Office, Chris and her female colleagues met with the President's wife, Mamie, who discussed meal planning and entertaining at the White House. It was at this time that Chris decided to pursue a career in a professional area, close to her heart, but rarely entered by women at that time: the biological sciences.
Accepted by multiple elite colleges, Chris chose to attend Goucher, a small women's college where she had immediate access to her aging grandparents. She continued her studies assiduously and began an independent research project on salt and water tolerance in a rare succulent plant, Ceropegia dichotoma.[19] She spent the summer of her junior year on a full fellowship at the Woods Hole Marine Biological Institute in Massachusetts, where she made important connections with faculty at both Harvard University and the University of Michigan.
After College, she spent a year and a half studying the largely unknown endemic insect fauna of the Canary Islands, Spain, supported by the National Science Foundation. At the same time, she collected literally thousands of rare plant specimens with Kornelius Lems, her college advisor. These plants were intended to become the basis of a Flora of the Canary Islands. Chris’ data and insect collections led to the completion of her PhD in 1970[20] in Zoology from the University of Michigan, where she was advised by Irving Cantrall and Theodore Hubbell. She was one of three PhD's awarded to women in her large class of young scientists. Following the accidental death of Kornelius in 1968, she completed her postdoctoral studies with Reed Rollins at Harvard University, where she wrote and illustrated Part One of the Technical Flora of the Canary Islands[21] and completed experiments on the evolution of growth form in Echium leucophaeum over an altitudinal gradient on La Palma Island.[22] Chris declined a tenure-track position at the University of Michigan to join her colleague and now husband, William Emmons Bradshaw, a like-minded, dedicated experimental biologist, who had a tenure-track position at the University of Oregon.
Joint Research
editIn 1971, William Bradshaw and Christina Holzapfel joined forces and moved to Oregon. Their joint research has been guided by two general principles: First, physiology provides the connection between the genome and the environment and second, a walk across geographic space is also a journey through evolutionary time.[23]
Several of many diverse aspects of their research findings have spanned the physics of light,[4] island biogeography,[24][25] habitat segregation and species coexistence in container environments,[26][27][28][29] gene-gene interactions (epistasis) underlying evolution in time and space,[30][31][32][33] and the integration of the two great biological timing mechanisms that orchestrate life on Earth: the daily circadian clock and the seasonal photoperiodic timer.[16][17][34][35][36][37] While the natural geographic range of the pitcher-plant mosquito has provided the backbone of their research, they have also studied container breeding tree-hole mosquitoes, using a grid of automobile tires as “ traps” placed in hardwood forests to sample overwintering populations from Florida to New England and from sea level to 1,000 metres (3,300 ft) in North Carolina[38][39] – even when the contents of tires were frozen. While sampling tree holes, they were drawn to the question of coexistence of multiple species in a finite habitat. They then showed that the traits permitting coexistence are genus level characters, and not the consequence of competitively driven, coevolved niche shifts among species, as was argued at that time.[40][41] They later confirmed this principle in British tree holes where the same genus-level traits persisted among different species and where a novel ground-water species was actively invading tree holes.[42][43][44] Unforeseen open niches exist, even in container habitats, let alone in more open ecological settings, thereby thwarting control measures through source reduction based on human-perceived constraints to mosquito habitat diversification.
Careful, repeated measurements of geographic variation in photoperiodic response over decades in eastern North America revealed one of their most startling discoveries: climate change has penetrated to the level of the gene and is driving evolution in the natural world in as few as five years.[45] This heritable change was later confirmed in other insects, plants, birds, and mammals.[4][5] Northern populations are becoming more southern-like, not by becoming more heat tolerant, but, in photoperiodic animals, by altered timing of seasonal development, reproduction, dormancy, and migration. Animals are not glaciers; it's seasonal timing that matters.[5][6][7] The revelation that climate change is driving evolution now permeates every aspect of life on Earth as we know it from agriculture and human health to global politics.
Their long experimental history with physiology, genetics, and evolution of photoperiodism over geography showed that the daily circadian clock and the seasonal photoperiodic timer not only can, but also do evolve independently over seasonal climatic gradients.[46][47][48] A fine-scale phylogeography involving over 40 populations and based on second-generation, high throughput sequencing[49] enabled overlaying photoperiodic response and its physiological properties on the actual genetic relatedness among populations. As a result, they demonstrated that any genetic constraints imposed by the daily circadian clock do not impede independent, rapid evolution of seasonal timing (photoperiodism) during range expansion or during periods of rapid climate change. The micro-evolutionary processes revealed within and among populations of W. smithii, programmed by a complex underlying genetic architecture, illustrate a gateway to the macro-evolutionary divergence of biological timing among species and higher taxa of insects.
All populations of the pitcher-plant mosquito exploit the same habitat and are fully interfertile from Florida to Newfoundland. Females mature their first batch of eggs without taking a blood meal; however, southern populations require blood for their second and subsequent batches, while evolutionarily derived northern populations are obligate non-blood feeding; yet, they produce multiple batches of eggs without ever biting.[20] Bradshaw, Holzapfel, their students, and multiple collaborators showed that the evolutionary transition from blood feeding to an obligate non-biting lifestyle was due to natural selection, rather than isolation and drift.[50][51][52][53][54] They showed that the evolution of nonbiting has resulted in a greatly reduced metabolic investment compared with biting populations, a greater reliance on opportunistic metabolic pathways, and greater reliance on visual rather than olfactory sensory input. Bradshaw and Holzapfel have been joined by colleagues at multiple universities, showing that there are important, overlapping metabolic pathways between the pitcher-plant mosquito associated with blood feeding and pathogen vectors, including Culex pipiens.[55] Together, they seek to control mosquito vectors of some of the world's most deadly pathogens, founded on the potent logic that if mosquitoes don't bite, they cannot spread disease.[56][57] This extension of their ongoing work has immense implications for the health and well-being of human populations, particularly in Third World, tropical regions where malaria alone devastates over 2,000,000 people annually.[58]
Awards
editTheir work has been supported continually by NSF and/or NIH for more than five decades. In 1986, they were awarded Guggenheim and Fulbright fellowships, along with National Geographic Society support, to compare mosquito population dynamics in Great Britain with corresponding populations in North America.[59][60][61][62]
In 2007, the Bradshaw and Holzapfel laboratory received its most distinguished commendation, being designated as one of 10 labs throughout all disciplines funded by the National Science Foundation (NSF) from astronomy and engineering to nanoscience and Earth sciences as best representing NSF's primary strategic outcome goal for DISCOVERY, to “Foster research that will advance the frontiers of knowledge, emphasizing areas of greatest opportunity and potential benefit and establishing the nation as a global leader in fundamental and transformational science and engineering.” “Knowledge gained from this research will assist in evaluating the survival of important agricultural crops, the spread of vector-borne diseases, the impact of agricultural pests, and the composition of natural biotic communities.” This commendation reflects not only Bradshaw and Holzapfel's persistent focus on photoperiodism as a central physiological process in an evolutionary context, but also highlights their strong collaborative efforts and continued productivity of their students.
In 2024, based on their contributions to mosquito biology and systematics, the American Mosquito Control Association, presented the Belkin Award to Holzapfel and Bradshaw, the first couple to receive this award jointly.
While remaining active in funded research, Holzapfel and Bradshaw are professor emerita and professor emeritus, respectively, in Biology at the University of Oregon.
Media Coverage
editTheir discovery that climate change has penetrated to the level of the gene and is driving evolution led to multiple interviews, including videos with NBC[63] and the Boston Globe,[64] print media with numerous newspaper and magazine articles, including Science,[65] The New Yorker,[10] and Time Magazine,[11] a book chapter (Kolbert,2006b),[40] as well as online from NSF.[41] Media coverage of the evolution of the biting phenotype in mosquitoes includes a highlight and commentary in PNAS [66][67] and a highlight in Natural History.[68]
Having trained well over 100 undergraduate research students over their long careers, Bill and Chris run their lab as a community of scholars,[69] providing independent research projects[70] for dedicated undergraduates in addition to the traditional training of graduate and post-doctoral students and hosting visiting scholars.
References
edit- ^ a b Bradshaw, William E. (March 24, 1972). "Action spectra for photoperiodic response in a diapausing mosquito" (PDF). Science. 175 (4028): 1361–1362. Bibcode:1972Sci...175.1361B. doi:10.1126/science.175.4028.1361. PMID 17813832.
- ^ Lems, Kornelius; Holzapfel, Christina (1974). Flora of the Canary Islands: The Cruciferae, the Crassulaceae, and the ferns and their allies. Annales del Instituto Nacional de Investigaciones Agrarias, Serie: Produción Vegetal (4 ed.). Instituto Nacional de Investigaciones Agrarias. pp. 165–273.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (December 4, 2001). "Genetic shift in photoperiodic response correlated with global warming" (PDF). Proceedings of the National Academy of Sciences USA. 98 (25): 14509–14511. doi:10.1073/pnas.241391498. PMC 64712. PMID 11698659.
- ^ a b Bradshaw, William E.; Holzapfel, Christina M. (June 9, 2006). "Climate change – Evolutionary response to rapid climate change" (PDF). Science. 312 (5779): 1477–1478. doi:10.1126/science.1127000. PMID 16763134.
- ^ a b c Bradshaw, William E.; Holzapfel, Christina M. (2008). "Genetic response to rapid climate change: it's seasonal timing that matters" (PDF). Molecular Ecology. 312 (1): 157–166. Bibcode:2008MolEc..17..157B. doi:10.1111/j.1365-294X.2007.03509.x. PMID 17850269.
- ^ a b Bradshaw, William E.; Holzapfel, Christina M. (2010). "Light, time, and the physiology of biotic response to rapid climate change in animals" (PDF). Annual Review of Physiology. 72: 147–166. doi:10.1146/annurev-physiol-021909-135837. PMID 20148671.
- ^ a b Bradshaw, William E.; Zani, Peter A.; Holzapfel, Christina M. (2004). "Adaptation to temperate climates" (PDF). Evolution. 58 (8): 1748–1762. doi:10.1111/j.0014-3820.2004.tb00458.x. PMID 15446427.
- ^ "Changing Mosquito Genes -- Changing Planet". U.S. National Science Foundation.
- ^ "Boston Globe". Bradshaw-Holzapfel Lab.
- ^ a b Kolbert, Elizabeth (January 9, 2006). "Butterfly lessons: Insects and toads respond to global warming". The New Yorker.
- ^ a b Walsh, Bryan (July 3, 2009). "Why are Scotland's sheep shrinking?". No. 174. Time.
- ^ Beck, Stanley D.; Alexander, Nancy (1964). "Proctodone, an insect developmental hormone". Biological Bulletin. 126 (2): 185–198. doi:10.2307/1539518. JSTOR 1539518.
- ^ Bradshaw, William E. (1970). "Interaction of food and photoperiod in the termination of larval diapause in Chaoborus americanus (Diptera: Culicidae)". Biological Bulletin. 139 (3): 476–484. doi:10.2307/1540366. JSTOR 1540366. PMID 5494233.
- ^ Bradshaw, William E. (1974). "Photoperiodic control of development in Chaoborus americanus with special reference to photoperiodic action spectra" (PDF). Biological Bulletin. 146 (1): 11–19. doi:10.2307/1540393. JSTOR 1540393. PMID 4150157.
- ^ a b Bradshaw, William E. (1973). "Homeostasis and polymorphism in vernal development of Chaoborus americanus". Ecology. 54 (6): 1247–1259. Bibcode:1973Ecol...54.1247B. doi:10.2307/1934187. hdl:2027.42/119057. JSTOR 1934187.
- ^ a b Bradshaw, William E. (1976). "Geography of photoperiodic response in a diapausing mosquito" (PDF). Nature. 262 (5567): 384–386. Bibcode:1976Natur.262..384B. doi:10.1038/262384b0. PMID 8725.
- ^ a b Bradshaw, William E.; Lounibos, L. Philip (1977). "Evolution of dormancy and its photoperiodic control in pitcher-plant mosquitoes" (PDF). Evolution. 31 (3): 546–567. doi:10.1111/j.1558-5646.1977.tb01044.x. PMID 28563474.
- ^ Lounibos, L.P.; Bradshaw, William E. (1975). "A second diapause in Wyeomyia smithii: seasonal incidence and maintenance by photoperiod" (PDF). Canadian Journal of Zoology. 53 (2): 215–221. doi:10.1139/z75-026. PMID 234786.
- ^ Lems, K.; Holzapfel, Christina M. (1963). "Botanical notes on the Canary Islands. IV. Cercopegia dichotoma (Asclepiadaceae), an unusual stem succulent". Boletin del Instituto Nacional de Investigaciones Agronómicas. 23 (48): 1–7.
- ^ Holzapfel, Christina M. (1970). "Zoogeography of the Acridoidea (Insecta Orthoptera) in the Canary Islands". ProQuest Dissertations & Theses Global.
- ^ Lems, Kornelius; Holzapfel, Christina (1974). Flora of the Canary Islands: The Cruciferae, the Crassulaceae, and the ferns and their allies. Annales del Instituto Nacional de Investigaciones Agrarias, Serie: Produción Vegetal (4 ed.). Instituto Nacional de Investigaciones Agrarias. pp. 165–273.
- ^ Lems, K.; Holzapfel, Christina M. (1971). "Adaptation of growth form in Echium leucophaeum (Boraginaceae)". Ecology. 52 (3): 499–506. Bibcode:1971Ecol...52..499L. doi:10.2307/1937633. JSTOR 1937633.
- ^ Bradshaw, William E.; Fletcher, M.C.; Holzapfel, Christina M. (2024). "Clock‑talk: have we forgotten about geographic variation?". Journal of Comparative Physiology A. 210 (4): 649–666. doi:10.1007/s00359-023-01643-9. PMC 11226528. PMID 37322375.
- ^ Holzapfel, Christina M. (1970). "Zoogeography of the Acridoidea (Insecta Orthoptera) in the Canary Islands". ProQuest Dissertations & Theses Global.
- ^ Lems, Kornelius; Holzapfel, Christina (1974). Flora of the Canary Islands: The Cruciferae, the Crassulaceae, and the ferns and their allies. Annales del Instituto Nacional de Investigaciones Agrarias, Serie: Produción Vegetal (4 ed.). Instituto Nacional de Investigaciones Agrarias. pp. 165–273.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (1983). "Predator-mediated, non-equilibrium coexistence of tree-hole mosquitoes in southeastern North America" (PDF). Oecologia (Berlin). 57 (1–2): 239–256. Bibcode:1983Oecol..57..239B. doi:10.1007/BF00379586. PMID 28310181.
- ^ MacArthur, Robert; Levins, Richard (1967). "The limiting similarity, convergence, and divergence of coexisting species". The American Naturalist. 101 (921): 377–385. doi:10.1086/282505.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (1992). "Resource limitation, habitat segregation, and species interactions of British tree-hole mosquitoes in nature". Oecologia. 90 (2): 227–237. Bibcode:1992Oecol..90..227B. doi:10.1007/BF00317180. PMID 28313718.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (1991). "Fitness and habitat segregation of British tree-hole mosquitoes. Ecological Entomology". Ecological Entomology. 16: 133–144. doi:10.1111/j.1365-2311.1991.tb00202.x.
- ^ Armbruster, Peter; Bradshaw, William E.; Holzapfel, Christina M. (1997). "Evolution of the genetic architecture underlying fitness in the pitcher-plant mosquito, Wyeomyia smithii" (PDF). Evolution. 51 (2): 451–458. doi:10.1111/j.1558-5646.1997.tb02432.x. PMID 28565340.
- ^ Bradshaw, William E.; Haggerty, Brian P.; Holzapfel, Christina M. (2005). "Epistasis underlying a fitness trait within a natural population of the pitcher-plant mosquito, Wyeomyia smithii" (PDF). Genetics. 169 (1): 485–488. doi:10.1534/genetics.104.031971. PMC 1448863. PMID 15466431.
- ^ Hard, Jeffrey J.; Bradshaw, William E.; Holzapfel, Christina M. (1993). "The genetic basis of photoperiodism and its evolutionary divergence among populations of the pitcher-plant mosquito, Wyeomyia smithii". The American Naturalist. 142 (3): 457–473. doi:10.1086/285549. PMID 19425986.
- ^ Lair, Kevin P.; Bradshaw, William E.; Holzapfel, Christina M. (1997). "Evolutionary divergence of the genetic architecture underlying photoperiodism in the pitcher-plant mosquito, Wyeomyia smithii". Genetics. 147 (4): 1873–1883. doi:10.1093/genetics/147.4.1873. PMC 1208353. PMID 9409843.
- ^ Bradshaw, William E.; Holzapfel, Christina M.; Mathias, D. (2006). "Circadian rhythmicity and photoperiodism in the pitcher-plant mosquito: Can the seasonal timer evolve independently of the circadian clock?" (PDF). The American Naturalist. 167 (4): 601–605. doi:10.1086/501032. PMID 16671002.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (2007). "Evolution of animal photoperiodism" (PDF). Annual Review of Ecology, Evolution and Systematics. 38: 1–25. doi:10.1146/annurev.ecolsys.37.091305.110115.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (2017). Natural variation and genetics of the photoperiodic timer in Wyeomyia smithii (PDF). Advances in Genetics. Vol. 99. pp. 39–71.
- ^ Bradshaw, William E.; Fletcher, M.C.; Holzapfel, Christina M. (2024). "Clock‑talk: have we forgotten about geographic variation?". Journal of Comparative Physiology A. 210 (4): 649–666. doi:10.1007/s00359-023-01643-9. PMC 11226528. PMID 37322375.
- ^ Holzapfel, Christina M.; Bradshaw, William E. (1981). "Geography of larval dormancy in the tree-hole mosquito, Aedes triseriatus (Say)" (PDF). Canadian Journal Zoology. 59 (6): 1014–1021. doi:10.1139/z81-141.
- ^ Bradshaw, W.E; Holzapfel, C.M. (1985). "The distribution and abundance of tree-hole mosquitoes in eastern North America: Perspectives from north Florida". In Rey, J.R.; Lounibos, L.P.; Frank, J.H. (eds.). Ecology of Mosquitoes: Proceedings of a Workshop. Vero Beach, FL.: Florida Medical Entomology Laboratories. pp. 3–23.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (1983). "Predator-mediated, non-equilibrium coexistence of tree-hole mosquitoes in southeastern North America" (PDF). Oecologia (Berlin). 57 (1–2): 239–256. Bibcode:1983Oecol..57..239B. doi:10.1007/BF00379586. PMID 28310181.
- ^ MacArthur, Robert; Levins, Richard (1967). "The limiting similarity, convergence, and divergence of coexisting species". The American Naturalist. 101 (921): 377–385. doi:10.1086/282505.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (1992). "Resource limitation, habitat segregation, and species interactions of British tree-hole mosquitoes in nature". Oecologia. 90 (2): 227–237. Bibcode:1992Oecol..90..227B. doi:10.1007/BF00317180. PMID 28313718.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (1991). "Fitness and habitat segregation of British tree-hole mosquitoes. Ecological Entomology". Ecological Entomology. 16: 133–144. doi:10.1111/j.1365-2311.1991.tb00202.x.
- ^ Holzapfel, Christina M.; Bradshaw, William E. (1986). "Habitat segregation among European tree-hole mosquitoes" (PDF). National Geographic Research. 2: 167–178.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (December 4, 2001). "Genetic shift in photoperiodic response correlated with global warming" (PDF). Proceedings of the National Academy of Sciences USA. 98 (25): 14509–14511. doi:10.1073/pnas.241391498. PMC 64712. PMID 11698659.
- ^ Bradshaw, William E.; Holzapfel, Christina M.; Mathias, D. (2006). "Circadian rhythmicity and photoperiodism in the pitcher-plant mosquito: Can the seasonal timer evolve independently of the circadian clock?" (PDF). The American Naturalist. 167 (4): 601–605. doi:10.1086/501032. PMID 16671002.
- ^ Bradshaw, William E.; Holzapfel, Christina M. (2017). Natural variation and genetics of the photoperiodic timer in Wyeomyia smithii (PDF). Advances in Genetics. Vol. 99. pp. 39–71.
- ^ Bradshaw, William E.; Fletcher, M.C.; Holzapfel, Christina M. (2024). "Clock‑talk: have we forgotten about geographic variation?". Journal of Comparative Physiology A. 210 (4): 649–666. doi:10.1007/s00359-023-01643-9. PMC 11226528. PMID 37322375.
- ^ Merz, C.; Catchen, J.M.; Hanson-Smith, V.; Emerson, K.J.; Bradshaw, William E.; Holzapfel, Christina M. (2013). "Replicate phylogenies and post-glacial range expansion of the pitcher-plant mosquito, Wyeomyia smithii, in North America". PLOS ONE 2013. 8 (e72262): e72262. Bibcode:2013PLoSO...872262M. doi:10.1371/journal.pone.0072262. PMC 3765167. PMID 24039746.
- ^ Bradshaw, William E.; Burkhart, J.; Colbourne, J.K.; Borowczak, R.; Lopez, J.; Denlinger, D.L.; Reynolds, J.A.; Pfrender, M.E.; Holzapfel, Christina M. (2018). "Evolutionary transition from blood feeding to obligate nonbiting in a mosquito". Proceedings of the National Academy of Sciences USA. 115 (5): 1009–1014. Bibcode:2018PNAS..115.1009B. doi:10.1073/pnas.1717502115. PMC 5798368. PMID 29255013.
- ^ Smith, S.M.; Brust, R.A.; Holzapfel, Christina M. (1971). "Photoperiodic control of the maintenance and termination of larval diapause in Wyeomyia smithii (Coq.) (Diptera: Culicidae) with notes on oogenesis in the adult female". Canadian Journal of Zoology. 49 (8): 1065–1073. doi:10.1139/z71-165. PMID 4398829.
- ^ Bradshaw, William E. (1980). "Blood-feeding and capacity for increase in the pitcher-plant mosquito, Wyeomyia smithii". Environmental Entomology. 9: 86–89. doi:10.1093/ee/9.1.86.
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