Xylem hydraulic evolution, I . W . B ailey, and N ardini & J ansen (2013): pattern and process

Scientific fields flourish when they enjoy an abundance of important hypotheses to test. It is hard for a field to grow if its aspiring students do not know what its main hypotheses are and where to find them.Notwithstanding, there is a persistent tradition in the comparative wood anatomical literature of attributing major causal evolutionary hypotheses to the prominent wood anatomist I.W. Bailey and his associates, even when their entire body of work of four decades (1918–1957) in fact contains no such hypotheses (Baas, 1976; Olson, 2012a). Sending aspiring students of xylem to Bailey for inspiration and direction does them a disservice because they will look in vain for the hypotheses in need of testing. For xylem studies to draw on a solid foundation, it is essential to understand what Bailey did accomplish as well as what he did not. A recent commentary (Nardini & Jansen, 2013, on Feild & Brodribb, 2013) raises an opportunity to examine the missing-inaction hypotheses in Bailey’s work regarding the evolutionary transition between scalariform and simple perforation plates. To examine this issue, I briefly summarize Baileyan thinking and contrast it with the main causal hypothesis that has been proposed to explain the scalariform-simple transition. I mention some of the important themes from Bailey’s work that find parallels in current xylem studies, comment on how to frame questions of evolutionary causes, and conclude by emphasizing that there are many interesting open questions in the study of the functional significance of variation in xylem structure. In 1918, Bailey and collaborator W. W. Tupper published a much-cited and rarely-read paper purporting to examine the relationship between cell size and trunk size across the woody plants. The study was burdened by the inconvenience that the authors neglected to gather the requisite stem size data. They noticed an interesting thing, though: the vessel elements that had scalariform perforation plates tended to be very long and narrow, whereas those with simple perforation plates were often very short and wide. By picking and choosing from across the ‘dicots’, Bailey and his associates found that they could line vessel elements up in a continual graded series from the longest scalariform plated elements to the shortest simple plated ones. Over a series of subsequent studies, they interpreted this long scalariform? short simple series as a ladder of evolutionary progress, concluding that simple perforation plates evolved via a progressive loss of bars from scalariform perforation plates (e.g. Frost, 1930). Simple perforation plates very well may have evolved from scalariform ones,meaning that Bailey andhis associates arrived atwhat could be a correct and important conclusion. While unquestionably an admirable inference, Bailey arrived at his conclusion via reasoning that was largely decades out of date even in 1918. Despite working in the early twentieth century, a time of much debate regarding the mechanisms of evolution (Gould, 2002; Shanahan, 2004), Bailey’s thinking was unaccountably pre-Darwinian. He believed fervently in ‘Haeckel’s law’ that ontogeny recapitulates phylogeny (Bailey, 1910; Frost, 1930). That doctrine had been conclusively rejected as a universal generalization by Bailey’s time (e.g. see the historical accounts of Russell, 1916 or De Beer, 1930). Bailey believed that evolution progressed via linear seriesmore at home inMedieval notions of the Great Chain of Being rather than the branching phylogenetic bush that had been de rigueur in evolutionary thinking for over 60 yr (Lovejoy, 1936; O’Hara, 1992; Bryant, 1995). He thought about the drivers of evolution in terms ofmurky notions of progress rather than mechanisms such as natural selection. Hardly justifiable notions even a century ago. Despite his shaky conceptual base, Bailey seems to have arrived at a potentially correct inference of the polarity of the scalariform? simple transition (though seeWheeler&Lehman, 2009). He anchored his inference of evolutionary transition in a case that just happened to fit his conceptual scheme. There are many plants that have scalariform perforation plates in the primary and firstformed secondary xylem but not in the later secondary xylem (many monocots, some Myristicaceae, etc.). That is, the ontogenetic transitions parallel the phylogenetic ones (see Mabee, 1989; Bryant, 1995). Bailey also employed what is now known as outgroup comparison, which reasons that given variation in the group of interest, the ingroup, the state not shared with the outgroup is the derived one (Kitching et al., 1998). In the flowering plants we find both vessel bearing and tracheid-bearing plants. The conifers have tracheids, so the possession of vessels in the flowering plants must be derived. Long scalariform-plated vessel elements look a lot like angiosperm tracheids, suggesting that the scalariform condition must be ancestral and the simple the derived one. The inference certainly seems a plausible one, even though in general ontogeny does not infallibly recapitulate phylogeny and even though evolution is manifestly not an inexorable linear progress. If evolution is not inexorable, then something must drive it. To look for a cause driving the scalariform-simple trend, we can now return to Nardini & Jansen (2013). In implying that Bailey ‘accounts for’ patterns of xylem evolution, Nardini & Jansen (2013) give readers the incorrect notion that there was any causal evolutionary content in Baileyan thinking. Evolutionary biologists study patterns in nature and try to infer something about the processes that generated them (e.g. Eldredge & Cracraft, 1980). The remarkable fit between