The scaling of expansive energy under the Red Queen predicts Cope’s Rule

The Red Queen’s hypothesis portrays evolution as a never-ending competition for expansive energy, where one species’ gain is another species’ loss. The Red Queen is neutral with respect to body size, implying that neither small nor large species have a universal competitive advantage. The maximum population growth in ecology; however, clearly depends on body size – the smaller the species, the shorter the generation length, and the faster it can expand. Here we ask whether, and if so how, the Red Queen’s hypothesis can accommodate a spectrum of body sizes. We theoretically analyse scaling of expansive energy with body mass and demonstrate that in the Red Queen’s zero-sum game for resources, neither small nor large species have a universal evolutionary advantage. We argue that smaller species have an evolutionary advantage only when resources in the environment are not fully occupied, such as after mass extinctions or following key innovations allowing expansion into freed up or previously unoccupied resource space. Under such circumstances, we claim, generation length is the main limiting factor for population growth. When competition for resources is weak, smaller species can indeed expand faster, but to sustain this growth they also need more resources. In the Red Queen’s realm, where resources are fully occupied and the only way for expansion is to outcompete other species, acquisition of expansive energy becomes the limiting factor and small species lose their physiological advantage. A gradual transition from unlimited resources to a zero-sum game offers a direct mechanistic explanation for observed body mass trends in the fossil record, known as Cope’s Rule. When the system is far from the limit of resources and competition is not maximally intense, small species take up ecological space faster. When the system approaches the limits of its carrying capacity and competition tightens, small species lose their evolutionary advantage and we observe a wider range of successful body masses, and, as a result, an increase in the average body mass within lineages.

Golden Orbweavers Ignore Biological Rules: Phylogenomic and Comparative Analyses Unravel a Complex Evolution of Sexual Size Dimorphism

Instances of sexual size dimorphism (SSD) provide the context for rigorous tests of biological rules of size evolution, such as Cope’s Rule (phyletic size increase), Rensch’s Rule (allometric patterns of male and female size), as well as male and female body size optima. In certain spider groups, such as the golden orbweavers (Nephilidae), extreme female-biased SSD (eSSD, female:male body length ≥ 2) is the norm. Nephilid genera construct webs of exaggerated proportions which can be aerial, arboricolous, or intermediate (hybrid). First, we established the backbone phylogeny of Nephilidae using 367 Anchored Hybrid Enrichment (AHE) markers, then combined these data with classical markers for a reference species-level phylogeny. Second, we used the phylogeny to test Cope and Rensch’s Rules, sex specific size optima, and the coevolution of web size, type, and features with female and male body size and their ratio, SSD. Male, but not female, size increases significantly over time, and refutes Cope’s Rule. Allometric analyses reject the converse, Rensch’s Rule. Male and female body sizes are uncorrelated. Female size evolution is random, but males evolve towards an optimum size (3.2–4.9 mm). Overall, female body size correlates positively with absolute web size. However, intermediate sized females build the largest webs (of the hybrid type), giant female Nephila and Trichonephila build smaller webs (of the aerial type), and the smallest females build the smallest webs (of the arboricolous type). We propose taxonomic changes based on the criteria of clade age, monophyly and exclusivity, classification information content, diagnosability, and arachnological community practice. We resurrect the family Nephilidae Simon 1894 that contains Clitaetra Simon 1889, the Cretaceous Geratonephila Poinar & Buckley 2012, Herennia Thorell 1877, Indoetra Kuntner 2006, new rank, Nephila Leach 1815, Nephilengys L. Koch 1872, Nephilingis Kuntner 2013, and Trichonephila Dahl 1911, new rank. We propose the new clade Orbipurae to contain Araneidae Clerck 1757, Phonognathidae Simon 1894, new rank, and Nephilidae. Nephilid female gigantism is a phylogenetically-ancient phenotype (over 100 ma), as is eSSD, though their magnitudes vary by lineage and, to some extent, biogeographically.

Dietary specialization is linked to reduced species durations in North American fossil canids

How traits influence species persistence is a fundamental question in ecology, evolution and palaeontology. We test the relationship between dietary traits and both species duration and locality coverage over 40 million years in North American canids, a clade with considerable ecomorphological disparity and a dense fossil record. Because ecomorphological generalization—broad resource use—may enable species to withstand disturbance, we predicted that canids of average size and mesocarnivory would exhibit longer durations and wider distributions than specialized larger or smaller species. Second, because locality coverage might reflect dispersal ability and/or survivability in a range of habitats, we predicted that high coverage would correspond with longer durations. We find a nonlinear relationship between species duration and degree of carnivory: species at either end of the carnivory spectrum tend to have shorter durations than mesocarnivores. Locality coverage shows no relationship with size, diet or duration. To test whether generalization (medium size, mesocarnivory) corresponds to an adaptive optimum, we fit trait evolution models to previously generated canid phylogenies. Our analyses identify no single optimum in size or diet. Instead, the primary model of size evolution is a classic Cope's Rule increase over time, while dietary evolution does not conform to a single model.

The dynamics of starvation and recovery

The eco-evolutionary dynamics of species are fundamentally linked to the energetic constraints of its constituent individuals. Of particular importance is the interplay between reproduction and the dynamics of starvation and recovery. To elucidate this interplay, we introduce a nutritional state-structured model that incorporates two classes of consumer: nutritionally replete, reproducing consumers, and undernourished, non-reproducing consumers. We obtain strong constraints on starvation and recovery rates by deriving allometric scaling relationships and find that population dynamics are typically driven to a steady state. Moreover, these rates fall within a ‘refuge’ in parameter space, where the probability of population extinction is minimized. We also show that our model provides a natural framework to predict maximum mammalian body size by determining the relative stability of an otherwise homogeneous population to a competing population with altered percent body fat. This framework provides a principled mechanism for a selective driver of Cope’s rule.