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Home , Evolutionary physiology

EDITORIAL

Evolutionary history and species interactions

Douglas J. Futuymaa,1 and Anurag A. Agrawalb aDepartment of and , Stony Brook University, Stony Brook, NY 11794-5245; and bDepartments of Ecology and and Entomology, and Cornell Center for a Sustainable Future, Cornell University, Corson Hall, Ithaca, NY 14853-2701

e celebrate this year the historical information. Well into the vide tests for the role of sesquicentennial anniver- 1970s, however, and sys- in ; and ‘‘gene trees’’ for re- sary of the publication of tematics were viewed by students of mi- lated species cast light on possible in- croevolution as descriptive sciences that stances of founder-effect speciation. A (1),W one of the most important books could contribute little to understanding phylogenetic framework is now de rigeur ever written. The two great themes of evolutionary processes—-a view that in addressing many, if not most, prob- The Origin are descent, with modifica- some paleontologists sought to dispel, lems in evolutionary biology (6). tion, of diverse species from common arguing that evolution includes processes An important and most interesting ancestors, and , which above the population level, such as dif- effect of being able to more confidently Darwin proposed as the chief agent of ferential rates of speciation and extinc- infer history is that evolutionary biolo- modification. He remarked, in Chapter tion (2, 3). On the whole, the study of gists have become more aware of the VI, that ‘‘it is generally acknowledged evolutionary history occupied a rela- role of historical explanation for the that all organic beings have been tively marginal position in evolutionary characteristics of living . This formed on two great laws—Unity of biology, which tended to be more fo- seems odd, because one would suppose Type, and the Conditions of Existence. cused on population-level processes. The that of all biological disciplines, evolu- By unity of type is meant that funda- divide between historical, generally mac- tionary biology should always have been mental agreement in structure, which we roevolutionary study and process- most conscious of the impact of history. see in organic beings of the same class, oriented, genetic, microevolutionary Nevertheless, an equilibrial assumption, and which is quite independent of their study was substantial (4). that organisms are near their adaptive habits of life. On my theory, unity of This situation has changed dramati- optima, has been widespread, arising in type is explained by unity of descent. cally in the last 15–20 years, owing part from evidence that most character- The expression of conditions of largely to the great growth in sophistica- istics are genetically variable and hence existence…is fully embraced by the prin- tion and reliability of , the responsive to natural selection, and in ciple of natural selection.’’ The two first task of which is to infer a major part from many examples of rapid great laws are conjoined, he noted, be- component of evolutionary history, to alterations of envi- cause natural selection will have namely the sequence of divergence of ronments. This assumption, which is adapted the parts of each being ‘‘during lineages as portrayed in phylogenetic characteristic of much of and long-past periods of time,’’ so that ‘‘the trees. Phylogenetic analysis of living or- functional (7), carried over law of the Conditions of Existence is the ganisms cannot entirely replace paleon- into ecology. For example, most com- higher law; as it includes, through the tology as a way of recovering the past; munity ecologists since the 1960s as- inheritance of former , that for example, it cannot reveal the exis- sumed that the species richness and of Unity of Type’’ (ref. 1, p. 168). tence of many extinct taxa. But it can species composition of ecological assem- Darwin thus described what we today provide insights into the history of taxa blages are near equilibrium, and could consider the main subjects of evolution- that are seldom fossilized. Moreover, it be explained by ecological theories ary biology: the history of evolution, enables us to trace the evolution of framed in terms of current and very including that history embodied in characters—-their polarity of change, recent environmental conditions (8). ‘‘unity of type,’’ the causal processes of convergence, reversal, elaboration—- Today, the theme of historical or ‘‘phy- evolution (including, but not only, natu- including molecular, physiological, be- logenetic constraints’’ looms large in ral selection), and the relation between havioral, and ecological features that are evolutionary biology, and ‘‘phylogenetic them. seldom recovered in fossils. Time- conservatism’’ of characters is thought During the 1930s and 1940s, dialogue calibrated phylogenies, incorporating not to account for many taxonomic patterns among geneticists, systematists, and pa- only the relative sequence but also the in ecological features such as habitat leontologists resulted in the ‘‘evolution- absolute time of lineage branching, en- associations (9). Likewise, community ary synthesis,’’ in which a chief point of able us to relate evolutionary events to ecologists increasingly recognize that the agreement was that the phenomena of climatic and geological changes (comple- diversity and identity of species in com- long-term evolution (‘‘,’’ menting paleontological data); to esti- munities, and the interactions among or ‘‘evolution above the species level’’) mate rates of character evolution; and to them, may be fully explicable only if result simply from the prolonged and infer the time course of diversification, long-term history, including macroevolu- repeated action of the processes of mu- including rates of speciation and extinc- tation, recombination, and gene fre- tion (5). It has become clear that histor- quency change that occur in populations ical information can often be used to Throughout 2009 PNAS will publish several collections of (‘‘’’). Despite this synthe- test hypotheses about evolutionary pro- articles examining various aspects of evolution and evolu- sis, evolutionary biology diverged into cess, based on the patterns that the hy- tionary theory. These collections include In Light of Evolu- tion III: Two Centuries of Darwin; , Changing largely disjunct studies of evolutionary potheses predict, so the once-divided Climate, and Niche Evolution; Out of Africa: Modern Hu- history (among species) and genetic pro- approaches are becoming united. For man Origins; Plant and Insect ; and Evolution in cesses (within species). Some inferences example, interspecific comparisons are Health and Medicine. about evolutionary history could be commonly used to detect selection at Author contributions: D.J.F. and A.A.A. wrote the paper. made from comparative studies by sys- the molecular level and to distinguish The authors declare no conflict of interest. tematists, but the fossil record was gen- modes of selection; contrasts between 1To whom correspondence should be addressed: E-mail: erally viewed as the chief source of the species richness of sister clades pro- [email protected].

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0910334106 PNAS ͉ October 27, 2009 ͉ vol. 106 ͉ no. 43 ͉ 18043–18044 Downloaded by guest on September 29, 2021 tionary history, is taken into account have arisen by a long history of coevolu- versely, understanding the ecology of (10, 11). For example, among the many tion that has affected the food web links communities of species requires appreci- hypotheses advanced to account for the between these trophic levels (16). Using ation of evolution and the role of greater species richness of many taxa in as data the host-plant associations and history. lower than higher latitudes, those that some physiological features of insects Darwin, whom many view as a include effects of long-term history ap- and the chemical and other defenses founder of ecology, appreciated that pear to be gaining favor (12). of plants—-features that are very imper- ‘‘plants and animals, most remote in The connections between community fectly documented by fossils—- the scale of nature, are bound together ecology and macroevolution are no- phylogenetic analyses enable us to by a web of complex relations’’ (ref. 1, where clearer than in interactions describe some aspects of the macroevo- p. 61). Since his time, we have learned among parasites and their hosts (13) and lution of these associations and relate quite a lot about the processes and his- among herbivores and their food plants them to contemporary interactions. tory whereby these relations have (14, 15), because many herbivores and Studies of herbivores and their host evolved. As the papers in this Special parasites are highly host-specific, and plants clearly show, as Reznick and Feature attest, evolution and ecology their host associations are often phylo- Ricklefs (17) recently urged, that ‘‘un- are indissolubly joined in the study of genetically conservative. More broadly, derstanding macroevolution requires the interactions between plants and their her- the diversity of herbivores, their host integration of ecology, evolution, and bivores, which offer a cardinal illustration plants, and the defensive adaptations of the role of history in shaping the diver- of evolution as the unifying theory of biol- plants to herbivory are postulated to sification or decline of lineages.’’ Con- ogy.

1. Darwin C (1859) On the Origin of Species by Means of 7. Garland T, Jr, Carter PA (1984) Evolutionary physiology. dinal diversity gradient: speciation, and bio- Natural Selection (Murray, London); reprinted (1996) Annu Rev Physiol 56:579–621. geography. Ecol Lett 10:315–331. (Oxford Univ Press, Oxford). 8. MacArthur RH (1972) Geographical Ecology: Patterns in 13. Poulin R, Morand S (2004) Parasite Biodiversity (Smith- 2. Raup DM, Gould SJ (1974) Stochastic simulation and the Distribution of Species (Harper and Row, New York). sonian, Washington, DC). evolution of morphology—-toward a nomothetic pa- 9. Wiens JJ, Graham CH (2005) Niche conservatism: Inte- 14. Mitter C, Brooks DR (1983) Phylogenetic aspects of leontology. Syst Zool 23:305–322. grating evolution, ecology, and . . Coevolution, eds Futuyma DJ, Slatkin M 3. Gould SJ (1980) The promise of paleobiology as a nomo- Annu Rev Ecol Evol Syst 36:519–539. (Sinauer, Sunderland, MA), pp 65–98. thetic, evolutionary discipline. Paleobiology 6:96–118. 10. Ricklefs RE, Schluter D (1993) Species diversity: regional 15. Mitter C, Farrell B, Futuyma DJ (1991) Phylogenetic 4. Futuyma DJ (1988) Sturm und Drang and the evolu- and historical influences. Species Diversity in Ecological studies of insect-plant interactions: Insights into the tionary synthesis. Evolution 42:217–226. Communities, eds Ricklefs RE, Schluter D (Univ of Chi- genesis of diversity. Trends Ecol Evol 6:290–293. 5. Nee S (2006) Birth-death models in macroevolution. cago Press, Chicago), pp 350–363. 16. Ehrlich PR, Raven PH (1964) Butterflies and plants: A Annu Rev Ecol Evol Syst 37:1–17. 11. Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW study in coevolution. Evolution 18:586–608. 6. Futuyma DJ (2004) The fruit of the . Assem- (2009) The merging of community ecology with phylo- 17. Reznick D, Ricklefs RE (2009) Darwin’s bridge between bling the Tree of Life, eds Cracraft J, Donoghue MJ genetic biology. Ecol Lett 12:693–715. microevolution and macroevolution. Nature 457:837– (Oxford Univ Press, Oxford), pp 25–39. 12. Mittelbach GG, et al. (2007) Evolution and the latitu- 842.

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