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

Abstract

Instances of sexual size dimorphism (SSD) provide the context for rigorous tests of biological rules of size evolution, such as Copes Rule (phyletic size increase), Renschs 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 to male body length exceeding 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 Renschs 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 Copes Rule. Allometric analyses reject the converse, Renschs 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.