Accounting for clinal variation and covariation in the assessment of taxonomic limits: why we should remember the ‘rules’

Well over a century has passed since the publication of a number of ideas that later became enshrined as biological ‘rules’: that endotherms tend to be larger in colder environments (‘Bergmann’s rule’; 1847, but see Salewski & Watt 2017), that the proportions of their external appendages change along the same temperature gradient (‘Allen’s rule’; 1877), and that they tend to be more heavily pigmented in more humid (wetter) environments (‘Gloger’s rule’; 1833). Although not rules in the strict sense of the word (Lawton 1999), these patterns appear to be general in nature, both within and between species, and they are not restricted to endotherms (e.g. James 1970, 1991, Graves 1991, James 1991, Teller ıa & Carbonell 1999, Ashton 2002, Guti errez-Pinto et al. 2014, Fan et al. 2019, Marcondes et al. 2020). They have generally been interpreted in the context of latitude or altitude; i.e. that animals are larger and paler and have relatively shorter appendages (wing, legs, tail, etc.) as their ranges approach the poles or at higher altitudes. However, environmental gradients, for example in temperature and rainfall, also vary with longitude or along other environmental axes, so such patterns may act in numerous directions. These broad patterns of gradual change across space are called clines, a term coined by Huxley (1938) and defined by him as ‘a gradation in measurable characters’. The drivers of clinal variation are not fully understood but are likely to reflect adaptation or phenotypic plasticity to local conditions that is to varying degrees dampened by gene flow between neighbouring populations. James (1991) argued that ‘the general concordance among species of birds in their clinal (gradual) patterns of geographic variation in size and color of plumage is so high that the primary regulatory process must be physiological adaptation to climate or its correlates’. Individuals at opposite ends of a cline may be genetically indistinguishable from one another, indicating that there is not necessarily a strong genetic component to clinal variation (Gardner et al. 2009, Husby et al. 2011, Ennen et al. 2014). Since the term was proposed, it has become increasingly clear that many, perhaps most, bird species exhibit clinal variation in their phenotypes across their ranges, including in song structure (e.g. Isler et al. 2009, Pitocchelli et al. 2018) and the prevalence of different colour morphs (Galeotti et al. 2003, Amar et al. 2014, Bosch 2019). Such variation may be apparent across very small geographical distances and even within populations on small islands (Wunderle 1981, Mil a et al. 2010). While clinal variation may often be subtle, with mean differences of just a few per cent between populations at opposite ends of the cline, it can also be extreme; for example, Line-cheeked Spinetail Cranioleuca antisiensis shows an almost three-fold variation in local mean body mass (from 11.5 to 31.0 g) across its elevational gradient (Seeholzer & Brumfield 2018). Thus, clinal variation in physical traits within taxa could easily exceed mean differences between taxa. Huxley hoped that the recognition of clinal variation would augment taxonomy, and that clines might constitute ‘a supplementary method which . would correct certain defects inherent in the naming of areal groups, notably in stressing continuity and regularity of variation as against mere distinctness of groups’. The extent to which his aspiration has been met is unclear. The Phylogenetic Species Concept (PSC) and the Biological Species Concept (BSC) generally use different approaches to define taxonomic limits; in crudely oversimplistic terms, the PSC approach tends to place greater emphasis on analyses of the genotype, the BSC approach on analyses of the phenotype. However, there is a general, and generally welcomed, trend towards a more integrative approach (e.g. Padial et al. 2010); taxa whose genotypes indicate that a revision of current taxonomic limits may be warranted are often subjected to corroborative analyses of phenotype, and vice versa. The case for revising taxonomic limits is greatly strengthened when variation in genotype and in phenotype align, although there is often considerable mismatch between the two (e.g. Alstr€ om et al. 2013, 2018, Drovetski et al. 2018). The literature now abounds with papers that compare phenotypic data between taxa, often in conjunction with analyses of genotype, and assume that statistically significant differences between taxa in plumage, structure, song or other traits are taxonomically informative. In particular, significant differences in phenotype between *Corresponding author. Email: paul.donald@birdlife.org