Mean body size in marine animals has increased more than 100-fold since the Cambrian, a discovery that brings to attention the key life-history parameters of lifespan and growth rate that ultimately determine size. Variation in these parameters is not well understood on the planet today, much less in deep time. Here, we present a new global database of maximum reported lifespan and shell growth coupled with body size data for 1 148 populations of marine bivalves and show that (i) lifespan increases, and growth rate decreases, with latitude, both across the group as a whole and within well-sampled species, (ii) growth rate, and hence metabolic rate, correlates inversely with lifespan, and (iii) opposing trends in lifespan and growth combined with high variance obviate any demonstrable pattern in body size with latitude. Our observations suggest that the proposed increase in metabolic activity and demonstrated increase in body size of organisms over the Phanerozoic should be accompanied by a concomitant shift towards faster growth and/or shorter lifespan in marine bivalves. This prediction, testable from the fossil record, may help to explain one of the more fundamental patterns in the evolutionary and ecological history of animal life on this planet.
One of the longest-lived, noncolonial animals on the planet today is a bivalve that attains life spans in excess of 500 years and lives in a cold, seasonally food-limited setting. Separating the influence of temperature and food availability on life span in modern settings is difficult, as these two conditions covary. The life spans of fossil animals can provide insights into the role of environment in the evolution of extreme longevity that are not available from studies of modern taxa. We examine bivalves from the unique, nonanalogue, warm and high-latitude setting of Seymour Island, Antarctica, during the greenhouse intervals of the Late Cretaceous and Paleogene. Despite significant sampling limitations, we find that all 11 species examined are both slow growing and long-lived, especially when compared with modern bivalves living in similar temperature settings. While cool temperatures have long been thought to be a key factor in promoting longevity, our findings suggest an important role for caloric restriction brought about by the low and seasonal light regime of the high latitudes. Our life-history data, spanning three different families, emphasize that longevity is in part governed by environmental rather than solely phylogenetic or ecologic factors. Such findings have implications for both modern and ancient latitudinal diversity gradients, as a common correlate of slow growth and long life is delayed reproduction, which limits the potential for evolutionary change. While life spans of modern bivalves are well studied, data on life spans of fossil bivalves are sparse and largely anecdotal. Life histories of organisms from deep time can not only elucidate the controls on life span but also add a new dimension to our understanding of macroevolutionary patterns.
Organismal metabolic rates reflect the interaction of environmental and physiological factors. Thus, calcifying organisms that record growth history can provide insight into both the ancient environments in which they lived and their own physiology and life history. However, interpreting them requires understanding which environmental factors have the greatest influence on growth rate and the extent to which evolutionary history constrains growth rates across lineages. We integrated satellite measurements of sea-surface temperature and chlorophyll-a concentration with a database of growth coefficients, body sizes, and life spans for 692 populations of living marine bivalves in 195 species, set within the context of a new maximum-likelihood phylogeny of bivalves. We find that environmental predictors overall explain only a small proportion of variation in growth coefficient across all species; temperature is a better predictor of growth coefficient than food supply, and growth coefficient is somewhat more variable at higher summer temperatures. Growth coefficients exhibit moderate phylogenetic signal, and taxonomic membership is a stronger predictor of growth coefficient than any environmental predictor, but phylogenetic inertia cannot fully explain the disjunction between our findings and the extensive body of work demonstrating strong environmental control on growth rates within taxa. Accounting for evolutionary history is critical when considering shells as historical archives. The weak relationship between variation in food supply and variation in growth coefficient in our data set is inconsistent with the hypothesis that the increase in mean body size through the Phanerozoic was driven by increasing productivity enabling faster growth rates.
Marine bivalves are well known for their impressive lifespans. Like trees, bivalves grow by accretion and record age and size throughout ontogeny in their shell. Bivalves, however, can form growth increments at several different periodicities depending on their local environment. Thus, establishing lifespans and growth rates of marine bivalves requires a proper identification of annual growth increments. Here, we use isotope sclerochronology to decipher the accretionary growth record of modern Astarte borealis from the White Sea, Russia (N 67°05.70′; E 32°40.85′). Unlike winter growth increments observed in many other cold-temperate and boreal bivalve and limpet species, prominent growth increments in A. borealis corresponded to the most negative values in the oxygen isotope (δ 18 O) time series indicating that they formed during summer. Furthermore, summer growth increments do not coincide with the external concentric ridges on the shell making the latter feature an unreliable indicator of age. Similar to many other polar bivalves, A. borealis shows slow growth and long life. The von Bertalanffy growth equation for our sample is H t = 29.39*(1 − e (− 0.11(t−(− 1.86)) ). Lifespans of individuals examined here (n = 18) range from 16 to 48 years. Given its impressive longevity and widespread polar distribution, A. borealis may be a potentially valuable skeletal archive for monitoring environmental conditions in the Arctic Ocean and boreal seas in the face of changing climate.
The field of sclerochronology has long been known to paleobiologists. Yet, despite the central role of growth rate, age, and body size in questions related to macroevolution and evolutionary ecology, these types of studies and the data they produce have received only episodic attention from paleobiologists since the field's inception in the 1960s. It is time to reconsider their potential. Not only can sclerochronological data help to address long-standing questions in paleobiology, but they can also bring to light new questions that would otherwise have been impossible to address. For example, growth rate and life-span data, the very data afforded by chronological growth increments, are essential to answer questions related not only to heterochrony and hence evolutionary mechanisms, but also to body size and organism energetics across the Phanerozoic. While numerous fossil organisms have accretionary skeletons, bivalves offer perhaps one of the most tangible and intriguing pathways forward, because they exhibit clear, typically annual, growth increments and they include some of the longest-lived, non-colonial animals on the planet. In addition to their longevity, modern bivalves also show a latitudinal gradient of increasing life span and decreasing growth rate with latitude that might be related to the latitudinal diversity gradient. Is this a recently developed phenomenon or has it characterized much of the group's history? When and how did extreme longevity evolve in the Bivalvia? What insights can the growth increments of fossil bivalves provide about hypotheses for energetics through time? In spite of the relative ease with which the tools of sclerochronology can be applied to these questions, paleobiologists have been slow to adopt sclerochronological approaches. Here, we lay out an argument and the methods for a path forward in paleobiology that uses sclerochronology to answer some of our most pressing questions.
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