22. Tilman, D. (2011), ‘Diversification, biotic interchange, and the universal trade-off hypothesis’, American Naturalist, 178, 355–71.
CHAPTER 7: EVOLUTION NEVER GIVES UP
1. Singer, M. C., Thomas, C. D. & Parmesan, C. (1993), ‘Rapid human-induced evolution of insect–host associations’, Nature, 366, 681–3.
2. The blue-eyed Marys are in the plant family Scrophulariaceae, and lousewort in the related plant family Orobanchaceae, hence they share some plant chemicals that make the switch possible. Evolution operates within a series of constraints, so they would not have been able to evolve to lay eggs on, and larvae to eat, lupins or pine trees in such a short space of time.
3. There was a genetic basis for the change; Singer, M. C., Ng, D. & Thomas, C. D. (1988), ‘Heritability of oviposition preference and its relationship to offspring performance within a single insect population’, Evolution, 42, 977–85.
4. Thomas C. D. (2005), ‘Recent evolutionary effects of climate change’, in Climate Change and Biodiversity, Lovejoy, T. E. & Hannah, L. (eds.), New Haven, CT: Yale University Press, pp. 75–88.
5. When I refer to ‘bursts’ and ‘spurts’ of evolution, I am referring to occasions when the rate of genotypic (the genes in each individual) change is relatively fast and results in rapid and substantial phenotypic change (in appearance, behaviour or physiology), which allows a population either to survive when conditions change, or to exploit new opportunities.
6. Severns, P. M. & Warren, A. D. (2008), ‘Selectively eliminating and conserving exotic plants to save an endangered butterfly from local extinction’, Animal Conservation, 11, 476–83; Severns, P. M. & Breed, G. A. (2014), ‘Behavioral consequences of exotic host plant adoption and the differing roles of male harassment on female movement in two checkerspot butterflies’, Behavioral Ecology & Sociobiology, 68, 805–14.
7. Bowers, M. D. & Richardson, L. L. (2013), ‘Use of two oviposition plants in populations of Euphydryas phaeton Drury (Nymphalidae)’, Journal of the Lepidopterists’ Society, 67, 299–300.
8. Graves, S. D. & Shapiro, A. M. (2003), ‘Exotics as host plants of the California butterfly fauna’, Biological Conservation, 110, 413–33.
9. Singer, M. C., Thomas, C. D. & Parmesan, C. (1993), ‘Rapid human-induced evolution of insect–host associations’, Nature, 366, 681–3.
10. Bourn, N. A. D. & Thomas, J. A. (1993), ‘The ecology and conservation of the brown argus butterfly Aricia agestis in Britain’, Biological Conservation, 63, 67–74.
11. Pateman, R. M. et al. (2012), ‘Temperature-dependent alterations in host use drive rapid range expansion in a butterfly’, Science, 336, 1028–30.
12. Thomas, C. D. et al. (2001), ‘Ecological and evolutionary processes at expanding range margins’ Nature, 411, 577–81; Buckley, J., Butlin, R. K. & Bridle, J. R. (2012), ‘Evidence for evolutionary change associated with the recent range expansion of the British butterfly, Aricia agestis, in response to climate change’, Molecular Ecology, 21, 267–80; Bridle, J. R. et al. (2014), ‘Evolution on the move: Specialization on widespread resources associated with rapid range expansion in response to climate change’, Proceedings of the Royal Society of London B: Biological Sciences, 281, 20131800; Buckley, J. & Bridle, J. R. (2014), ‘Loss of adaptive variation during evolutionary responses to climate change’, Ecology Letters, 17, 1316–25.
13. As of December 2016, the international Paris climate change agreement aims to keep the average global temperature below 2°C (and preferably closer to 1.5°C) above pre-industrial conditions. However, the individual country pledges made to date are expected to lead to warming of approximately 2.7°C, if they are all fulfilled.
14. This is akin to the geneticist’s concept of a ‘ring species’, where there is a geographic continuum of populations, each of which can reproduce with its neighbours, but if the extreme ends of the continuum meet up, they operate as though they are separate species.
15. Phillipps, Q. & Phillipps, K. (2014), ‘Phillipps’ Field Guide to the Birds of Borneo, Oxford: John Beaufoy Publishing (3rd edition).
16. Laland, K. N., Odling-Smee, F. J. & Myles, S. (2010), ‘How culture shaped the human genome: Bringing genetics and the human sciences together’, Nature Reviews Genetics, 11, 137–48.
17. Hooke, R. L., Martín-Duque, J. F. & Pedraza, J. (2012), ‘Land transformation by humans: A review’, GSA Today, 22, 4–10.
18. Carroll, S. P. et al. (2007), ‘Evolution on ecological time-scales, Functional Ecology, 21, 387–93.
19. Darimont, C. T. et al. (2009), ‘Human predators outpace other agents of trait change in the wild’, Proceedings of the National Academy of Sciences, USA, 106, 952–4.
20. Hemingway, J. & Ranson, H. (2000), ‘Insecticide resistance in insect vectors of human disease’, Annual Review of Entomology, 45, 371–91.
21. Roush, R. & Tabashnik, B. E. (eds.) (2012), Pesticide Resistance in Arthropods, Springer Science & Business Media.
22. Heap, I. (2014), ‘Herbicide resistant weeds’, in Integrated Pest Management, pp. 281–301, Netherlands: Springer.
23. Pelz, H. J. et al. (2005), ‘The genetic basis of resistance to anticoagulants in rodents’ Genetics, 170, 1839–47.
24. Berthold, P. et al. (1992), ‘Rapid microevolution of migratory behaviour in a wild bird species’, Nature, 360, 668–70; Karell, P. et al. (2011), ‘Climate change drives microevolution in a wild bird’, Nature Communications, 2, 208.
25. Hill, J. K., Griffiths, H. M. & Thomas, C. D. (2011), ‘Climate change and evolutionary adaptations at species’ range margins’, Annual Review of Entomology, 56, 143–59.
26. Phillips, B. L. et al. (2006), ‘Invasion and the evolution of speed in toads’, Nature, 439, 803.
27. Saccheri, I. J. et al. (2008), ‘Selection and gene flow on a diminishing cline of melanic peppered moths’, Proceedings of the National Academy of Sciences, USA, 105, 16212–17.
28. Antonovics, J., Bradshaw, A. D. & Turner, R. G. (1971), ‘Heavy metal tolerance in plants’, Advances in Ecological Research 7, 1–85.
CHAPTER 8: THE PANGEAN ARCHIPELAGO
1. Arbogast, B. S. et al. (2006), ‘The origin and diversification of Galapagos mockingbirds’, Evolution 60, 370–82; Nietlisbach, P. et al. (2013), ‘Hybrid ancestry of an island subspecies of Galápagos mockingbird explains discordant gene trees’, Molecular Phylogenetics and Evolution, 69, 581–92.
2. Durham, W. H. (2012), ‘What Darwin found convincing in Galápagos’, The Role of Science for Conservation, 34, 1.
3. As new islands are continuously emerging as a result of volcanic activity and then erode away, the first colonists may actually have arrived on Galapagos islands that are now submerged.
4. Some further exchange of individuals would continue (gene flow), but immigration of new individuals from another island would be very small, relative to the size of the resident population on each island. Thus, the populations on each island could continue to diverge–although there would be potential for genes that are beneficial on all islands to spread between them.
5. Grant, P. R. & Grant, B. R. (2011), How and Why Species Multiply: The Radiation of Darwin’s Finches, Princeton, New Jersey: Princeton University Press.
6. Lamichhaney, S. et al. (2015), ‘Evolution of Darwin’s finches and their beaks revealed by genome sequencing’, Nature, 518, 371–5.
7. Lerner, H. R. et al. (2011), ‘Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers’, Current Biology, 21, 1838–44.
8. The process of evolution into separate species in isolated geographic locations is known as ‘allopatric speciation’.
9. Including New Zealand, but excluding New Guinea, which already supported terrestrial mammals. Once a species is flightless, it may lose the ability to colonize new islands (though not completely: volcanic activity, plate tectonics, coral growth and sea-level changes may connect and then disconnect islands).
10. Tilman, D. (2011), ‘Diversi
fication, biotic interchange, and the universal trade-off hypothesis’, American Naturalist, 178, 355–71.
11. This excludes South American deer species that also live in Central and North America. The taxonomy of South American deer is still debated, so the final ‘agreed’ number of species may be slightly higher or lower than fourteen.
12. In the rodent subfamily Sigmodontinae.
13. Hughes, C. & Eastwood, R. (2006), ‘Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes’, Proceedings of the National Academy of Sciences USA, 103, 10334–9; Nevado, B. et al. (2016), ‘Widespread adaptive evolution during repeated evolutionary radiations in New World lupins’, Nature Communications, 7, 12384.
14. Tilman, D. (2011), ‘Diversification, biotic interchange, and the universal trade-off hypothesis’, American Naturalist, 178, 355–71.
15. Zuk, M., Simmons, L. W. & Cupp, L. (1993), ‘Calling characteristics of parasitized and unparasitized populations of the field cricket Teleogryllus oceanicus’, Behavioral Ecology and Sociobiology, 33, 339–43.
16. Zuk, M., Rotenberry, J. T. & Tinghitella, R. M. (2006), ‘Silent night: Adaptive disappearance of a sexual signal in a parasitized population of field crickets’, Biology Letters, 2, 521–4.
17. Johnston, R. F. & Selander, R. K. (1964), ‘House sparrows: Rapid evolution of races in North America’, Science, 144, 548–50; Schrey, A. W. et al. (2011), ‘Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow (Passer domesticus) populations’, Molecular Ecology, 20, 1133–43; Liebl, A. L. et al. (2015), ‘Invasion genetics: Lessons from a ubiquitous bird, the house sparrow Passer domesticus’, Current Zoology, 61, 465–76; Huey, R. B. et al. (2000), ‘Rapid evolution of a geographic cline in size in an introduced fly’, Science, 287, 308–9; Balanyá, J. et al. (2006), ‘Global genetic change tracks global climate warming in Drosophila subobscura’, Science, 313, 1773–5.
18. Langkilde, T. (2009), ‘Invasive fire ants alter behavior and morphology of native lizards’, Ecology, 90, 208–17.
19. Some seeds may survive for several years before they germinate, so the total number of generations may be less than the number of years.
20. Montesinos, D., Santiago, G. & Callaway, R. M. (2012), ‘Neo-allopatry and rapid reproductive isolation’, American Naturalist, 180, 529–33.
21. Feder J. L. (1998), in Howard D. J. & Berlocher S. H. (eds.), Endless Forms: Species and Speciation, New York: Oxford University Press; Feder, J. L. et al. (2003), ‘Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella’, Genetics, 163, 939–53.
22. The first apple orchard in North America was planted in 1625, in Boston. However, the evolution of the apple fly is not likely to have commenced until the continent-wide proliferation of apples during the nineteenth century.
23. Forbes, A. A. et al. (2009), ‘Sequential sympatric speciation across trophic levels’, Science, 323, 776–9; Hood, G. R. et al. (2015), ‘Sequential divergence and the multiplicative origin of community diversity’, Proceedings of the National Academy of Sciences USA, 112, E5980–E5989.
24. It is now accepted that one species can sometimes turn into two in the absence of geographic separation of the populations, a process known as sympatric speciation. The frequency of these events is still debated, as well as whether apple flies are quite ‘there’ yet. Berlocher, S. H. & Feder, J. L. (2002), ‘Sympatric speciation in phytophagous insects: Moving beyond controversy?’, Annual Review of Entomology, 47, 773–815.
25. Geneticists do not all agree on the definition of a species: some prefer a definition in which there is (almost) no possibility of successful reproduction with other species (the apple fly has not yet reached this stage); others consider separate species to be ‘types’ that remain distinct, despite some ongoing mating and gene flow between the two (the apple fly has apparently reached this stage).
CHAPTER 9: HYBRID
1. Harris, S. A. (2002), ‘Introduction of Oxford ragwort, Senecio squalidus L. (Asteraceae), to the United Kingdom’, Watsonia, 24, 31–43.
2. Not everyone would count it as a ‘full species’, but it is a self-perpetuating genetic form that no longer interbreeds with its parental species through geographic isolation; Abbott, R. J. et al. (2003), ‘Plant introductions, hybridization and gene flow’, Philosophical Transactions of the Royal Society B, 358, 1123–32; Abbott, R. J. et al. (2009), ‘Recent hybrid origin and invasion of the British Isles by a self-incompatible species, Oxford ragwort (Senecio squalidus L., Asteraceae)’, Biological Invasions, 11, 1145–58.
3. Lowe, A. J. & Abbott, R. J. (2004), ‘Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)’, Heredity, 92, 386–95; Abbott, R. J. & Lowe, A. J. (2004), ‘Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles’, Biological Journal of the Linnean Society, 82, 467–74.
4. Abbott, R. J. & Lowe, A. J. (2004), ‘Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles’, Biological Journal of the Linnean Society, 82, 467–74; Hegarty, M. J., Abbott, R. J. & Hiscock, S. J. (2012), ‘Allopolyploid speciation in action: The origins and evolution of Senecio cambrensis’, in Soltis, P. S. & Soltis, D. E. (eds.), Polyploidy and Genome Evolution, pp. 245–70, Heidelberg: Springer.
5. Ainouche, M. & Gray, A. (2016), ‘Invasive Spartina: Lessons and challenges’, Biological Invasions, 18, 2119–22.
6. Thomas, C. D. (2015), ‘Rapid acceleration of plant speciation during the Anthropocene’, Trends in Ecology & Evolution, 30, 448–55.
7. This calculation is based on multiplying up the world land surface, excluding ice and deserts. This number should be regarded as an order-of-magnitude estimate.
8. Many of these hybrids are between so-called ‘native’ species, but many ‘native’ British plants live where they do only because humans have altered the landscape and transported species for millennia.
9. Milne, R. I. & Abbott, R. J. (2000), ‘Origin and evolution of invasive naturalized material of Rhododendron ponticum L. in the British Isles’, Molecular Ecology, 9, 541–56.
10. Matsuoka, Y. (2011), ‘Evolution of polyploid Triticum wheats under cultivation: The role of domestication, natural hybridization and allopolyploid speciation in their diversification’, Plant & Cell Physiology, 52, 750–64.
11. Seijo, G. et al. (2007), ‘Genomic relationships between the cultivated peanut (Arachis hypogaea, Leguminosae) and its close relatives revealed by double GISH’, American Journal of Botany, 94, 1963–71.
12. Schmidt, R. & Bancroft, I. (eds.) (2011), Genetics and Genomics of the Brassicaceae, New York: Springer-Verlag.
13. Soltis, P. S. & Soltis, D. E. (2009), ‘The role of hybridization in plant speciation’, Annual Review of Plant Biology, 60, 561–88.
14. Morgan-Richards, M. et al. (2004), ‘Interspecific hybridization among Hieracium species in New Zealand: Evidence from flow cytometry’, Heredity, 93, 34–42.
15. Sankararaman, S. et al. (2014), ‘The genomic landscape of Neanderthal ancestry in present-day humans’, Nature, 507, 354–7.
16. Huerta-Sánchez, E. et al. (2014), ‘Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA’, Nature, 512, 194–7; Harrison, R. G. & Larson, E. L. (2014), ‘Hybridization, introgression, and the nature of species boundaries’, Journal of Heredity, 105 (S1), 795–809.
17. Mavárez, J. et al. (2006), ‘Speciation by hybridization in Heliconius butterflies’, Nature, 441, 868–71; Arias, C. F. et al. (2014), ‘Phylogeography of Heliconius cydno and its closest relatives: Disentangling their origin and diversification’, Molecular Ecology, 23, 4137–52; Heliconius Genome Consortium (2012), ‘Butterfly genome reveals promiscuous exchange of mimicry adaptations among species’, Nature, 487, 94–8; Kozak, K. M. et al. (2015), ‘Multilocus spec
ies trees show the recent adaptive radiation of the mimetic Heliconius butterflies’, Systematic Biology, syv007.
18. Pollinger, J. P. et al. (2011), ‘A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids’, Genome Research, 21, 1294–305.
19. Scriber, J. M., & Ording, G. J. (2005), ‘Ecological speciation without host plant specialization: Possible origins of a recently described cryptic Papilio species’, Entomologia Experimentalis et Applicata, 115, 247–63; Cong, Q. et al. (2015), ‘Tiger swallowtail genome reveals mechanisms for speciation and caterpillar chemical defense’, Cell Reports, 16, 910–19.
20. Amaral, A. R. et al. (2014), ‘Hybrid speciation in a marine mammal: The Clymene dolphin (Stenella clymene)’, PLOS ONE, 9, e83645.
21. Miller, W. et al. (2012), ‘Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change’, Proceedings of the National Academy of Sciences USA, 109, E2382–E2390; Cahill, J. A. et al. (2015), ‘Genomic evidence of geographically widespread effect of gene flow from polar bears into brown bears’, Molecular Ecology, 24, 1205–17.
22. Gogarten, J. P., Doolittle, W. F. & Lawrence, J. G. (2002), ‘Prokaryotic evolution in light of gene transfer’, Molecular Biology and Evolution, 19, 2226–38.
23. Schwarz, D. et al. (2007), ‘A novel preference for an invasive plant as a mechanism for animal hybrid speciation’, Evolution, 61, 245–56.
24. Schwarz, D. et al. (2005), ‘Host shift to an invasive plant triggers rapid animal hybrid speciation’, Nature, 436, 546–9.
25. Senn, H. V. & Pemberton, J. M. (2009), ‘Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area’, Molecular Ecology, 18, 862–76.
26. http://www.nonnativespecies.org/factsheet/downloadFactsheet.cfm?speciesId=725.
27. Hedrick, P. W. (2009), ‘Conservation genetics and North American bison (Bison bison)’, Journal of Heredity, 100, 411–20.
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