Abstract
Dwarfing, an adaptive evolutionary process1 by which the descendant grows to a smaller adult size than its ancestor, may evolve as a byproduct of selection acting primarily on LH characteristics, particularly on age at sexual maturity2 (ASM). LH theory posits that a small adult size can result from either advancement or postponement of sexual maturity, depending on the ecological scenario3,4,5. Broadly speaking, high extrinsic mortality (predation, parasite loads) curtails the time-period of growth (truncation) by forcing an early channeling of resources from growth to reproduction6, which results in growth arrest and an advanced onset of sexual maturity; the organism is small-at-maturity. Low resource availability, by contrast, forces a reduction in the rate of growth2,7, generally associated with prolonged allocation of resources to maintenance6,7 and a correlated delay in sexual maturity2,4,8; the organism remains small-for-age throughout ontogeny. Rate and duration of growth, hence, are the two variables (at least in determinate growers) that mediate the pace of life in response to prevailing environmental conditions.
Dwarfing is a ubiquitous phenomenon that is particularly pervasive on islands where it affects large mammals and dinosaurs and, to a lesser extent, other vertebrates and even plants9,10,11,12,13. Insular dwarfing is now widely considered to be an adaptive response to selection pressures imposed by environmental conditions where net primary production and, hence, per capita food resources are low, and/or under elevated population density2,14,15,16,17,18,19,20,
Among herbivores, elephants have the slowest relative GRs29. Elephants form a group of very large mammals characterized by a slow LH with a slow GR, delayed age at maturity and long lifespan; indeed, they commonly live longer than 60 years in the wild30. Along with humans, they represent the slow end of the slow-fast LH continuum among terrestrial mammals, which is usually depicted as a mouse—elephant continuum. Through the scaling with body mass, their slow life-history is a direct result of their gigantic size. Unsurprisingly, hence, it is intuitively assumed that ‘dwarfed giants’ shifted towards a faster LH as in the case of P. falconeri23 from the late Middle Pleistocene of Sicily (Spinagallo cave, Syracuse, Supplementary material 1). At just 0.9 to 1.2 m tall, and with an estimated mean body mass of 252 kg (Supplementary material 2; Supplementary Tables 1, 2, 3), P. falconeri is the smallest elephant to have ever evolved; it weighted little more than 2% of its ancestor P. antiquus (11,500 kg31). Raia and colleagues23 calculated discrete LH values from interspecific scaling. Accordingly, the dwarf elephant attained sexual maturity at the age of 3–4 years, pregnancy took 189 days, and life span was 26 years. They considered a fast LH to be supported by an elevated number of unfused long bones interpreted as high calf mortality, and by the high number of tuskless females that supposedly arrested tusk growth to divert resources to reproduction. Because of their higher mass estimation for P. falconeri, Larramendi and Palombo25 provide similar but somewhat higher values. Roth21 suggested dwarfing in P. falconeri to be a consequence of selection for reduced energy use (through scaling of metabolic rate with body mass) and calculated a shortened growth period of 4 years based on body mass scaling. She furthermore speculated that by retention of a relatively long gestation period at a smaller body size, twins might have been more frequent than singletons. In current literature, P. falconeri is still being used as an example of evolution towards the fast end of the slow-fast LH continuum associated with insular dwarfing28.
In this study, we reconstruct the key LH traits ‘age at maturity’ and ‘longevity’, as well as the rate and duration of growth in P. falconeri from a histological analysis of bones (skeletochronology; beginning of the external fundamental system EFS; accretional bone area), molars (daily enamel secretion rate ESR; enamel extension rate EER; plate formation time PFT; crown formation time CFT), and tusks (dentine daily secretion rate DSR; dentine extension rate DER; first FOI, second SOI, and third TOI order increments), using multiple technical (microscopy, 3D imaging) and statistical (von Bertalanffy; segmented regression) tools. We perform phylogenetic generalized least square regressions (PGLS) to evaluate potential phylogenetic signals in allometric life-history/body mass analyses of P. falconeri, extant ungulates and elephants. We rely on external measurements and 178 histological slides from 29 tibiae, 1 upper fourth deciduous tooth, 1 lower third molar, and 6 tusks. We compare the resulting LH data with those from the extant, full-sized continental cousin Loxodonta africana and, as far as available, with PFT of fossil continental Mammuthus columbi32 P. antiquus (own data), and insular P. cypriotes32, to establish whether P. falconeri dwarfed via growth truncation or GR reduction (see “Materials and methods”). In doing so, we aim to bring the first comprehensive data on insular dwarf elephant LHs to bear on the debate over causality between the process of dwarfing and the evolution of LH strategies on islands.
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