The Editors of the Journal of Ecology are pleased to honour Professor Mark Westoby in our continuing Eminent Ecologist virtual issue series. The virtual issue is available on the Journal of Ecology website.
Assistant Editor, Journal of Ecology
How to interpret it when a trait is phylogenetically conservative
Westoby, M., M.R. Leishman and J.M. Lord. 1995. On misinterpreting the “phylogenetic correction”. Journal of Ecology 83:531-534.
Cornwell W, Westoby M, Falster DS, Fitzjohn R, O’Meara B, Pennell M, McGlinn D, Eastman J, Moles A, Reich PB, Tank D, Wright IJ, Aarssen L, Beaulieu J, Kooyman R, Leishman M, Miller E, Niinemets U, Oleksyn J, Ordonez A, Royer D, Mith S, Stevens P, Warman L, Wilf P, Zanne AE. 2014. Functional distinctiveness of major plant lineages. Journal of Ecology 102: 345-356
Westoby et al 1995 was a Forum item, the first paper in a longer exchange (Ackerly & Donoghue 1995; Harvey, Read & Nee 1995a; b; Rees 1995; Westoby, Leishman & Lord 1995a; b; c). It arose from the review process for Leishman et al 1995 (listed above under “seeds, dispersal biology, seedling establishment”). During that process a reviewer asserted that correlations of traits across species were no longer statistically legitimate and had been superseded by correlations of phylogenetic divergences. I wrote a more spelled-out explanation of our position in correspondence to the editor, then Jonathan Silvertown. Although he personally disagreed, he decided to accept the Leishman et al manuscript and to have the issues aired as an exchange. He invited Harvey to contradict us, and various others chimed in as the exchange went along.
Currently it’s again becoming more common to hear the claim that analysis of species trait data is required to be “phylogenetically informed”. You hear it even from editors of BES journals, who ought to know better. The crux of the issue is simple enough. For most traits, variation across species is correlated both with ecology (other traits, or habitat variables) and with phylogeny. That is, families or genera often have distinct ecological propensities. What happens when we consider ecology and phylogeny as potential causes or interpretations? – remembering always that correlation does not by itself prove causation. The important point is that ecology and phylogeny are not mutually exclusive causes. Species have both a phylogenetic history and an ecological competence in the present day, and correlation with one does not exclude causation by the other. So any analysis that takes phylogenetically conservative trait variation and removes it from consideration as potentially ecologically relevant must be misleading. In effect, such analyses are saying that differences between major clades can not be ecologically meaningful.
Janice Lord was a postdoc in the Macquarie lab working on the phylogenetic pattern in seed size (Lord, Westoby & Leishman 1995) and on accessory costs of seed production (Lord & Westoby 2006, 2012). She is now an academic at U Otago in New Zealand, and has given the Cockayne Memorial Lectures in 2015.
Cornwell et al 2014 mapped traits onto phylogeny with a view to describing specifics of evolutionary history, rather than from a perspective of statistically correcting for cross-correlation. It arose from a working group organised by Will Cornwell and Amy Zanne and supported mainly by the US National Evolutionary Synthesis Centre, with a meeting also in Australia supported by Macquarie Uni. At the time the working group got under way, trait data had accumulated for more than 10K species across several traits. The working group compiled a data set that spanned five main traits plus a number of others with lesser coverage, and focused on the question how different traits had radiated in relation to each other. Cornwell et al 2014 identified evolutionary divergences that were most influential for the breadth of trait variation observed in the present day (an idea prefigured in Moles et al. 2005, but using a different index of importance). The effect was to take very traditional knowledge, about the characters and lifestyles of particular clades, and put it on a freshly quantitative basis. For example Proteaceae were ranked 1 for increasing the spread of leaf N and SLA, Magnoliidae ranked 1 for leaf size and 2 seed size.
Macquarie lab people among the authors of Cornwell et al 2014 (besides Wright and Leishman who have already been mentioned) included Cornwell, Zanne and Fitzjohn. Will Cornwell did part of his Stanford PhD working from our lab, and was a frequent visitor as a postdoc though never formally enrolled or employed at Macquarie. He subsequently spent time at U British Columbia and Vrije Universiteit Amsterdam and is now a senior lecturer at U of New South Wales, across the other side of Sydney. Amy Zanne came to Macquarie as a postdoc with NSF International funding. She subsequently went to U Missouri St Louis and is now an Assoc Prof at George Washington U in Washington DC. She has continuing research collaborations in Australia. Both Will and Amy are members of the J Ecol Editorial Board.
Rich Fitzjohn spent postdoc time at Macquarie on a computing project and is now an app developer in ecology of diseases at Imperial College London.
Falster, Kooyman, Miller and Moles all did PhDs in the Macquarie lab at various times.
Daniel Falster is currently a postdoc at Macquarie and won the 2015 Next-Generation Ecologist Award from Ecological Society of Australia. Rob Kooyman lives in rainforest on the north coast of NSW (his PhD was undertaken after a long career as rainforest expert). He does research both with our lab and with the Royal Bot Gardens in Sydney. Angela Moles is now a professor at U New South Wales, and was Australia’s Life Scientist of the Year in 2013. Eliot Miller is a postdoc at the Cornell Ornithology Lab.
Looking back over this set of papers, they’re actually not too bad a representation of our lab’s interests overall, despite the big chance element about which pieces of work ended up in J Ecol rather than somewhere else. Probably the clearest trajectory corresponds to what’s become known as trait ecology. Of course all ecology and physiology is in some sense about traits (except maybe neutral theory). But the point about comparing trait constellations across many species is to put particular species and mechanisms in a wider context – to ask more quantitatively what “model systems” actually represent.
For us trait ecology began with work focused around seed size and its connections to other traits and to habitat (Jurado et al. 1991; Leishman & Westoby 1992; Hughes et al. 1994; Leishman et al. 1995). In the mid-90s a general agenda was formulated to approach plant strategies via trait axes (Westoby 1998; a paper that proved influential eventually, after being declined as insufficiently interesting by J Ecol and also by Ecology). Our attention expanded to leaf traits (e.g. Wright & Westoby 2002) and subsequently to stem traits (e.g. Falster & Westoby 2005). In parallel we began to assemble data sets to assess consistency across different continents and vegetation types (e.g. Leishman et al. 1995), leading eventually to the global communal-property datasets spanning tens of thousands of species that underpin many recent syntheses.
But the reason traits influence fitness, ultimately, is because of how they shape life histories and demography, and how those mesh with different disturbance regimes. So I’d see the self-thinning rule – how biomass accumulation translates into competitive mortality – as part of the same picture, and also the state-and-transition models for vegetation, and the demography in arid zones. Indeed self-thinning reappears in our recent models of traits in vegetation (e.g. Falster et al. 2011).
And finally I’d just like to apologise for leaving out all the people from our lab who have worked on fish, on mammal habitats, on insect communities, on gene conflict and cooperation, or who for whatever other reason have somehow gotten through life without sending papers to Journal of Ecology.
Prof. Mark Westoby
Ackerly, D.D. & Donoghue, M.J. (1995) Phylogeny and ecology reconsidered. J. Ecol., 83, 730–733.
Beadle, N.C.W. (1954) Soil phosphate and the delimitation of plant communities in eastern Australia. Ecology, 35, 370–375.
Beadle, N.C.W. (1962) Soil phosphate and the delimitation of plant communities in eastern Australia II. Ecology, 43, 281–288.
Benson, D. & Howell, J. (1995) Taken for Granted: The Bushland of Sydney and Its Suburbs. Kangaroo Press.
Cunningham, S.A., Summerhayes, B. & Westoby, M. (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecological Monographs, 69, 569–588.
Eldridge, D., Westoby, M. & Holbrook, K. (1991) Soil surface characteristics, microtopography and proximity to mature shrubs: effects on survival of several cohorts of Atriplex vesicaria seedlings. J Ecol, 79, 357–364.
Falster, D.S., Brännström, Å., Dieckmann, U. & Westoby, M. (2011) Influence of four major plant traits on average height, leaf-area cover, net primary productivity, and biomass density in single-species forests: a theoretical investigation. Journal of Ecology, 99, 148–164.
Falster, D.S. & Westoby, M. (2005) Alternative height strategies among 45 dicot rain forest species from tropical Queensland, Australia. Journal of Ecology, 93, 521–535.
Fonseca, C.R., Overton, J.M., Collins, B. & Westoby, M. (2000) Shifts in trait-combinations along rainfall and phosphorus gradients. Journal of Ecology, 88, 964–977.
Grime, J.P. (1979) Plant Strategies and Vegetation Processes. Wiley, Chichester.
Grime, J.P. & Hunt, R. (1975) Relative growth-rate: its range and adaptive significance in a local flora. J. Ecol., 63, 393–422.
Harper, J.L. (1967) A Darwinian approach to plant ecology. Journal of Ecology, 55, 247–270.
Harvey, P.H., Read, A.F. & Nee, S. (1995a) Why ecologists need to be phylogenetically challenged. J. Ecol., 83, 535–536.
Harvey, P.H., Read, A.F. & Nee, S. (1995b) Further remarks on the role of phylogeny in comparative ecology. J. Ecol., 83, 733–734.
Hill, R.S. (1998) Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Australian Systematic Botany, 11, 391–400.
Howell, J. & Benson, D.H. (2000) Sydney’s Bushland: More Than Meets the Eye. Royal Botanic Gardens & Domain Trust – Sydney.
Hughes, L., Dunlop, M., French, K., Leishman, M.R., Rice, B., Rodgerson, L. & Westoby, M. (1994) Predicting dispersal spectra: a minimal set of hypotheses based on plant attributes. J. Ecol., 82, 933–950.
Jurado, E. & Westoby, M. (1992) Seedling growth in relation to seed size among species of arid Australia. Journal of Ecology, 80, 407–416.
Jurado, E., Westoby, M. & Nelson, D. (1991) Diaspore weight, dispersal, growth form and perenniality of central Australian plants. Journal of Ecology, 79, 811–830.
Lambers, H. & Poorter, H. (1992) Inherent variation in growth rate between higher plants: a search for ecological causes and consequences. Adv. Ecol. Res., 23, 187–261.
Leishman, M. & Westoby, M. (1992) Classifying plants into groups on the basis of associations of individual traits — evidence from Australian semi-arid woodlands. J Ecol, 80, 417–424.
Leishman, M.R. & Westoby, M. (1994a) The role of seed size in seedling establishment in dry soil conditions – experimental evidence from semi-arid species. Journal of Ecology, 82, 249–258.
Leishman, M.R. & Westoby, M. (1994b) Hypotheses On Seed Size – Tests Using the Semiarid Flora of Western New-South-Wales, Australia. American Naturalist, 143, 890–906.
Leishman, M.R., Westoby, M. & Jurado, E. (1995) Correlates of seed size variation: a comparison among five temperate floras. Journal of Ecology, 83, 517–529.
Lord, J.M. & Westoby, M. (2006) Accessory costs of seed production. Oecologia, 150, 310–317.
Lord, J.M. & Westoby, M. (2012) Accessory Costs of Seed Production and the Evolution of Angiosperms. Evolution, 66, 200–210.
Lord, J., Westoby, M. & Leishman, M. (1995) Seed size and phylogeny in six temperate floras: constraints, niche conservatism, and adaptation. Am. Nat., 146, 349–364.
Moles, A.T., Ackerly, D.D., Webb, C.O., Tweddle, J.C., Dickie, J.B. & Westoby, M. (2005) A brief history of seed size. Science, 307, 576–580.
Moles, A.T., Falster, D.S., Leishman, M.R. & Westoby, M. (2004) Small-seeded species produce more seeds per square metre of canopy per year, but not per individual per lifetime. Journal of Ecology, 92, 384–396.
Moles, A.T. & Westoby, M. (2004) Seedling survival and seed size: a synthesis of the literature. Journal of Ecology, 92, 372–383.
Noy-Meir, I. (1973) Desert ecosystems: environment and producers. Annual Review of Ecology and Systematics, 4, 25–51.
Rees, M. (1995) EC-PC Comparative Analyses? Journal of Ecology, 83, 891–893.
Saverimuttu, T. & Westoby, M. (1996) Seedling longevity under deep shade in relation to seed size. Journal of Ecology, 84, 681–689.
Tadaki, Y. & Shidei, T. (1959) Studies on the competition of forest trees. II. The thinning experiment on small model stand of Sugi (Cryptomeria japonica) seedlings. Nippon Rin Gakkaishi, 41, 341–349.
Vesk, P.A. & Westoby, M. (2004) Sprouting ability across diverse disturbances and vegetation types worldwide. Journal of Ecology, 92, 310–320.
Watson, I.W., Westoby, M. & Holm, A.M. (1997a) Demography of two shrub species from an arid grazed ecosystem in Western Australia 1983-93. Journal of Ecology, 85, 815–832.
Watson, I.W., Westoby, M. & Holm, A.M. (1997b) Continuous and episodic components of demographic change in arid zone shrubs: models of two Eremophila species from Western Australia compared with published data from other species. Journal of Ecology, 85, 833–846.
Westoby, M. (1980) Relations between genet and tiller population dynamics: tiller survival under clipping in Phalaris tuberosa. J Ecol, 68, 683–870.
Westoby, M. (1981) The place of the self-thinning rule in population dynamics. Amer. Nat., 118, 581–587.
Westoby, M. (1982) Frequency distributions of plant size during competitive growth of stands: the operation of distribution-modifying-functions. Ann. Bot., 50, 733–735.
Westoby, M. (1984) The self-thinning rule. Advances in Ecological Research, 14, 167–226.
Westoby, M. (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant and Soil, 199, 213–227.
Westoby, M. & Howell, J. (1981) Self-thinning: the effect of shading on glasshouse populations of silver beet (Beta vulgaris). J Ecol, 69, 359–366.
Westoby, M. & Howell, J. (1986) The influence of population structure on self-thinning. J Ecol, 74, 343–359.
Westoby, M., Leishman, M. & Lord, J.M. (1995a) Further remarks on phylogenetic correction. J. Ecol., 83, 727–734.
Westoby, M., Leishman, M.R. & Lord, J.M. (1995b) On misinterpreting the “phylogenetic correction.” J. Ecol., 83, 531–534.
Westoby, M., Leishman, M.R. & Lord, J.M. (1995c) Issues of interpretation after relating comparative datasets to phylogeny. J. Ecol., 83, 892–893.
Westoby, M., Moles, A.T. & Falster, D.S. (2009) Evolutionary coordination between offspring size at independence and adult size. Journal of Ecology, 97, 23–26.
Wright, I.J., Reich, P.B. & Westoby, M. (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf lifespan. Journal of Ecology, 90, 534–543.
Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, J.H.C., Diemer, M., Flexas, J., Garnier, E., Groom, P.K., Gulias, J., Hikosaka, K., Lamont, B.B., Lee, T., Lee, W., Lusk, C., Midgley, J.J., Navas, M.L., Niinemets, U., Oleksyn, J., Osada, N., Poorter, H., Poot, P., Prior, L., Pyankov, V.I., Roumet, C., Thomas, S.C., Tjoelker, M.G., Veneklaas, E.J. & Villar, R. (2004) The worldwide leaf economics spectrum. Nature, 428, 821–827.
Wright, I.J. & Westoby, M. (1999) Differences in seedling growth behaviour among species: trait correlations across species, and trait shifts along nutrient compared to rain gradients. Journal of Ecology, 87, 85–97.
Wright, I.J. & Westoby, M. (2002) Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytologist, 155, 403–416.
Yoda, K., Kira, T., Ogawa, H. & Hozumi, H. (1963) Self-thinning in overcrowded pure stands under cultivated and natural conditions. J Inst Polytech Osaka City Univ Series D, 14, 107–129.
Zammit, C. & Westoby, M. (1988) Predispersal seed losses and the survival of seeds and seedlings of two serotinous Banksia shrubs in burnt and unburnt heath. J Ecol, 76, 200–214.