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 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 \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{upgreek} \usepackage{mathrsfs} \setlength{\oddsidemargin}{-69pt} \begin{document} }{}$\ge$\end{document} 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 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 toward 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, and diagnosability. Spider families, as currently defined, tend to be between 37 million years old and 98 million years old, and Nephilidae is estimated at 133 Ma (97–146), thus deserving family status. We, therefore, resurrect the family Nephilidae Simon 1894 that contains Clitaetra Simon 1889, the Cretaceous Geratonephila Poinar and Buckley (2012) , Herennia Thorell 1877, Indoetra Kuntner 2006 , new rank, Nephila Leach 1815, Nephilengys L. Koch 1872, Nephilingis Kuntner 2013, Palaeonephila Wunderlich 2004 from Tertiary Baltic amber, 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 lineag...

Caribbean golden orbweaving spiders maintain gene flow with North America

“…To identify the best priors for the reconstruction of ultrametric phylogenies, we performed stepping‐stone sampling and Bayes factor test (Baele et al, ) within BEAST2 (Bouckaert et al, ). We reduced the total data set (Table ) and constrained the topology according to a phylogenomic hypothesis (Kuntner et al, ). Model tests (Note ) selected a strict clock with the rate 0.0112 (Bidegaray‐Batista & Arnedo, ) and a coalescent constant population tree prior.…”

“…Our present study thus focuses on the nephilid genus Trichonephila Dahl in the Caribbean. Trichonephila is a global genus of golden orbweavers (Nephilidae) that contains species known to readily cross long, overwater distances (Kuntner et al, ). Only two species are currently known in the New World, with T. clavipes distributed widely from North to South America (Kuntner, ).…”

Phylogeny of the orb‐weaving spider family Araneidae (Araneae: Araneoidea)

“…Note: Kuntner et al. () transferred all Nephila species figured here to Trichonephila . [Colour figure can be viewed at wileyonlinelibrary.com]…”

“…Kuntner et al. () found Nephila to be polyphyletic, resurrected an old genus ( Trichonephila ) name to apply to the non‐ Nephila moiety, and another ( Indoetra ) for the sister to Clitaetra , resulting in seven nephiline genera. For most of the 20 th century and before, Nephila and its relatives were considered as a subfamily of Araneidae until Levi () suggested a placement within Tetragnathidae.…”

“…Since then Nephila and its relatives have been moved back and forth between Tetragnathidae and Araneidae, or placed in their own family, Nephilidae (Kuntner, ). The latest phylogenetic and phylogenomic analyses placed Nephila and its relatives as sister to Araneidae (Dimitrov et al., ; Garrison et al., ; Wheeler et al., ; Fernández et al., ; Kuntner et al., ) or nested within Araneidae (Kuntner et al., ; Dimitrov et al., ; Kallal et al., ). Kallal and Hormiga () included the araneid genus Paraplectanoides and found strong support for a sister‐group relationship to nephilines.…”