Matjaž Kuntner

Bioprospecting Finds the Toughest Biological Material: Extraordinary Silk from a Giant Riverine Orb Spider

Background Combining high strength and elasticity, spider silks are exceptionally tough, i.e., able to absorb massive kinetic energy before breaking. Spider silk is therefore a model polymer for development of high performance biomimetic fibers. There are over 41.000 described species of spiders, most spinning multiple types of silk. Thus we have available some 200.000+ unique silks that may cover an amazing breadth of material properties. To date, however, silks from only a few tens of species have been characterized, most chosen haphazardly as model organisms (Nephila) or simply from researchers backyards. Are we limited to ‘blindly fishing’ in efforts to discover extraordinary silks? Or, could scientists use ecology to predict which species are likely to spin silks exhibiting exceptional performance properties? Methodology We examined the biomechanical properties of silk produced by the remarkable Malagasy ‘Darwins bark spider’ (Caerostris darwini), which we predicted would produce exceptional silk based upon its amazing web. The spider constructs its giant orb web (up to 2.8 m2) suspended above streams, rivers, and lakes. It attaches the web to substrates on each riverbank by anchor threads as long as 25 meters. Dragline silk from both Caerostris webs and forcibly pulled silk, exhibits an extraordinary combination of high tensile strength and elasticity previously unknown for spider silk. The toughness of forcibly silked fibers averages 350 MJ/m3, with some samples reaching 520 MJ/m3. Thus, C. darwini silk is more than twice tougher than any previously described silk, and over 10 times better than Kevlar®. Caerostris capture spiral silk is similarly exceptionally tough. Conclusions Caerostris darwini produces the toughest known biomaterial. We hypothesize that this extraordinary toughness coevolved with the unusual ecology and web architecture of these spiders, decreasing the likelihood of bridgelines breaking and collapsing the web into the river. This hypothesis predicts that rapid change in material properties of silk co-occurred with ecological shifts within the genus, and can thus be tested by combining material science, behavioral observations, and phylogenetics. Our findings highlight the potential benefits of natural history–informed bioprospecting to discover silks, as well as other materials, with novel and exceptional properties to serve as models in biomimicry.

Phylogeny of Extant Nephilid Orb-Weaving Spiders (Araneae, Nephilidae): Testing Morphological and Ethological Homologies

The Pantropical spider clade Nephilidae is famous for its extreme sexual size dimorphism, for constructing the largest orb‐webs known, and for unusual sexual behaviors, which include emasculation and extreme polygamy. We synthesize the available data for the genera Nephila, Nephilengys, Herennia and Clitaetra to produce the first species level phylogeny of the family. We score 231 characters (197 morphological, 34 behavioral) for 61 taxa: 32 of the 37 known nephilid species plus two Phonognatha and one Deliochus species, 10 tetragnathid outgroups, nine araneids, and one genus each of Nesticidae, Theridiidae, Theridiosomatidae, Linyphiidae, Pimoidae, Uloboridae and Deinopidae. Four most parsimonious trees resulted, among which successive weighting preferred one ingroup topology. Neither an analysis of an alternative data set based on different morphological interpretations, nor separate analyses of morphology and behavior are superior to the total evidence analysis, which we therefore propose as the working hypothesis of nephilid relationships, and the basis for classification. Ingroup generic relationships are (Clitaetra (Herennia (Nephila, Nephilengys))). Deliochus and Phonognatha group with Araneidae rather than Nephilidae. Nephilidae is sister to all other araneoids (contra most recent literature). Ethological data, although difficult to obtain and thus frequently missing for rare taxa, are phylogenetically informative. We explore the evolution of selected morphological and behavioral characters, discuss and redefine the homology of palpal sclerites, disprove semientelegyny in spiders, trace the newly interpreted evolution of the orb web, and show that nephilid genital morphologies coevolve with sexual behaviors and extreme sexual size dimorphism. Phylogenetic interpretations of behavior suggest new insights into spider biology and avenues for future research.

Dogs, cats, and kin: a molecular species-level phylogeny of Carnivora.

Phylogenies underpin comparative biology as high-utility tools to test evolutionary and biogeographic hypotheses, inform on conservation strategies, and reveal the age and evolutionary histories of traits and lineages. As tools, most powerful are those phylogenies that contain all, or nearly all, of the taxa of a given group. Despite their obvious utility, such phylogenies, other than summary supertrees, are currently lacking for most mammalian orders, including the order Carnivora. Carnivora consists of about 270 extant species including most of the worlds large terrestrial predators (e.g., the big cats, wolves, bears), as well as many of mans favorite wild (panda, cheetah, tiger) and domesticated animals (dog, cat). Distributed globally, carnivores are highly diverse ecologically, having occupied all major habitat types on the planet and being diverse in traits such as sociality, communication, body/brain size, and foraging ecology. Thus, numerous studies continue to address comparative questions within the order, highlighting the need for a detailed species-level phylogeny. Here we present a phylogeny of Carnivora that increases taxon sampling density from 28% in the most detailed primary-data study to date, to 82% containing 243 taxa (222 extant species, 17 subspecies). In addition to extant species, we sampled four extinct species: American cheetah, saber-toothed cat, cave bear and the giant short-faced bear. Bayesian analysis of cytochrome b sequences data-mined from GenBank results in a phylogenetic hypothesis that is largely congruent with prior studies based on fewer taxa but more characters. We find support for the monophyly of Carnivora, its major division into Caniformia and Feliformia, and for all but one family within the order. The only exception is the placement of the kinkajou outside Procyonidae, however, prior studies have already cast doubt on its family placement. In contrast, at the subfamily and genus level, our results indicate numerous problems with current classification. Our results also propose new, controversial hypotheses, such as the possible placement of the red panda (Ailuridae) sister to canids (Canidae). Our results confirm previous findings suggesting that the dog was domesticated from the Eurasian wolf (Canis lupus lupus) and are congruent with the Near East domestication of the cat. In sum, this study presents the most detailed species-level phylogeny of Carnivora to date and a much needed tool for comparative studies of carnivoran species. To demonstrate one such use, we perform a phylogenetic analysis of evolutionary distinctiveness (EDGE), which can be used to help establish conservation priorities. According with those criteria, and under one of the many possible sets of parameters, the highest priority Carnivora species for conservation of evolutionary diversity include: monk seals, giant and red panda, giant otter, otter civet, Owstons palm civet, sea otter, Liberian mongoose, spectacled bear, walrus, binturong, and the fossa.

The Form and Function of Spider Orb Webs: Evolution from Silk to Ecosystems

Spiders are the preeminent silk craftsmen among arthropods and are best known for producing aerial orb webs that snare flying insects. Orb web spiders are ubiquitous predators in terrestrial ecosystems and are popular models for behavioural and ecological research, in part due to the ease of characterizing the shapes of orb webs. Orb webs are composite structures built from multiple types of silks, each with its own unique molecular structure and mechanical function, such that orb webs also link together evolutionary research from the genes coding for silk proteins to whole web function in the environment. Yet, orb webs are only intermediate structures in the evolutionary diversification of silk use among spiders, acting as stepping stones facilitating the origin of new web types and increased spider diversification. Here, we review the current research on the form and function of spider orb webs. We provide a comprehensive introduction to all aspects of orb web biology, suitable for any new investigation into orb web biology. While other reviews exist individually for webs, silk, and spider evolution, we hope that the synthetic nature of this review will facilitate a more integrated approach by future investigators. Finally, we explore in more detail some of the most dynamic areas of orb web biology to suggest promising venues for the next decade of research on these fascinating creatures and their silken snares. In particular, we discuss how spider webs might drive speciation, the dramatic growth in our understanding of the molecular ecology of spider silk, and the importance of a greater role for spider biology per se in silk biomimicry.

Madagascar: an unexpected hotspot of social Anelosimus spider diversity (Araneae: Theridiidae)

Abstract.u2002 The spider genus Anelosimus Simon, 1891 (Theridiidae) currently contains over forty described species, found worldwide in tropical to warm temperate areas. American Anelosimus are all social, a rare trait among spiders, but social behaviour has not been reported for Anelosimus species elsewhere. Old World Anelosimus are poorly known, both behaviourally and taxonomically, and no Anelosimus species have yet been described from sub‐Saharan Africa or Madagascar. Based on a preliminary phylogenetic analysis we predicted sociality in an undescribed Madagascar species because it grouped among social New World species. An expedition to Madagascar then found no less than five undescribed periodic‐social (subsocial) Anelosimus species in Périnet reserve. A sixth species from the same locality is known from museum specimens and the Anelosimus diversity of Périnet is comparable with the most diverse single locality in the Americas. Subsocial species play a key role in understanding the evolution of permanent sociality (quasisociality). This increased pool of available subsocial study species demonstrates the utility of phylogenies as predictors of traits in species thus far unstudied. Here, A. andasibesp.n., A.u2003may Agnarsson sp.n., A. nazarianisp.n., A. salleesp.n., A. salutsp.n. and A. vondronasp.n. are described. Anelosimus locketi Roberts, 1977 from Aldabra Atoll is a junior synonym of A. decaryi ( Fage, 1930 ) comb.n. from Madagascar. Preliminary data on the behaviour of the new species are given, indicating a level of sociality similar to the American A.‘arizona’1. The phylogenetic analysis supports the monophyly of the Madagascar group and places it as sister to a clade containing the eximius lineage from the Americas, and a pair of undescribed Tanzanian species.

Ecology and web allometry of Clitaetra irenae, an arboricolous African orb-weaving spider (Araneae, Araneoidea, Nephilidae)

Abstract Analysis of ecological data of the arboricolous nephilid spider Clitaetra irenae Kuntner 2006, endemic to Maputaland forests, South Africa, indicates the species dependence on this highly threatened habitat. We tested C. irenae habitat dependence via GIS analysis by plotting the known distribution against southern African ecoregions. In the southern part of its range, C. irenae inhabits almost exclusively one ecoregion, the Maputaland coastal plain forests; but further north, in tropical southern Africa, it continues inland into Malawis woodlands. We test and refute the hypotheses that C. irenae inhabits exclusively mature trees, trees of a particular species, trees with a smooth bark, tree habitats at certain height above ground, and only closed canopy forest stands. The ecological niche of C. irenae is flexible as long as suitable trees under at least partially closed canopy are available. We quantify the C. irenae ontogenetic web changes from orb to ladder and the simultaneous hub displacement towards the top frame. Such web allometry allows the web to increase vertically but not horizontally, which enables the spider to remain on the same tree throughout its development and thus the ladder web architecture is an adaptation to an arboricolous life style. Adult hub displacement, common in spiders with vertical webs, is explained by gravity. Clitaetra irenae web orientation on trees correlates with forest closure, and might indicate the Maputaland forest quality. We argue for utilization of the ecology of arboricolous nephilid orb-weaving spiders (Clitaetra and Herennia) in systematic conservation assessments in the Old World tropics.

The Generation of a Biodiversity Hotspot: Biogeography and Phylogeography of the Western Indian Ocean Islands

The importance of islands in revealing evolutionary processes was highlighted already at the birth of evolutionary biology as a science (Darwin 1859; Darwin and Wallace 1858). Since the thrilling discoveries revealed by Darwin’s work on the Galapagos (Darwin 1909) and Wallace’s work in the Malay (Indonesian) archipelago (Wallace 1876), island biogeography has experienced an explosive growth. The discipline has provided many elegant examples of the evolutionary mechanisms involved in generating biodiversity, especially the interplay of geological processes and colonization and isolation (Emerson 2008; Gillespie, Claridge, and Goodacre 2008; Parent, Caccone, and Petren 2008; Ricklefs and Bermingham 2008). Islands have provided particularly strong insights into adaptive radiations (Camacho-Garcia and Gosliner 2008; Blackledge and Gillespie 2004; Cowie and Holland 2008; Gillespie and Roderick 2002; Losos and DeQueiroz 1997; Schluter 2000), the processes of colonization and extinction (Ricklefs and Bermingham 2008; Goldberg, Lancaster, and Ree 2011), the formation of species (Emerson 2008; Pickford et al. 2008; Gillespie and Roderick 2002; Schluter and Nagel 1995; Vences et al. 2009), and convergent evolution and formation of ecomorphs (Bossuyt and Milinkovitch 2000; Gillespie 2004, 2005; Losos 1988; Wildman et al. 2007; Burridge 2000; Rothe et al. 2011). Naturally, islands have also played a key role in revealing the causes and consequences of long distance dispersal, in particular, the ecological and evolutionary consequences of varying dispersal propensities of different lineages, and the evolutionary changes in dispersal propensity, such as the loss of dispersal ability following island colonization (Cowie and Holland 2006, 2008; Hedges and Heinicke 2007; Holland and Cowie 2006; Byrne et al. 2011; Bell et al. 2005; Darwin 1909; Clark 1994; Gillespie et al. 2012).

Mass predicts web asymmetry in Nephila spiders

The architecture of vertical aerial orb webs may be affected by spider size and gravity or by the available web space, in addition to phylogenetic and/or developmental factors. Vertical orb web asymmetry measured by hub displacement has been shown to increase in bigger and heavier spiders; however, previous studies have mostly focused on adult and subadult spiders or on several size classes with measured size parameters but no mass. Both estimations are suboptimal because (1) adult orb web spiders may not invest heavily in optimal web construction, whereas juveniles do; (2) size class/developmental stage is difficult to estimate in the field and is thus subjective, and (3) mass scales differently to size and is therefore more important in predicting aerial foraging success due to gravity. We studied vertical web asymmetry in a giant orb web spider, Nephila pilipes, across a wide range of size classes/developmental stages and tested the hypothesis that vertical web asymmetry (measured as hub displacement) is affected by gravity. On a sample of 100 webs, we found that hubs were more displaced in heavier and larger juveniles and that spider mass explained vertical web asymmetry better than other measures of spider size (carapace and leg lengths, developmental stage). Quantifying web shape via the ladder index suggested that, unlike in other nephilid taxa, growing Nephila orbs do not become vertically elongated. We conclude that the ontogenetic pattern of progressive vertical web asymmetry in Nephila can be explained by optimal foraging due to gravity, to which the opposing selective force may be high web-building costs in the lower orb. Recent literature finds little support for alternative explanations of ontogenetic orb web allometry such as the size limitation hypothesis and the biogenetic law.

THE AFRICAN SPIDER GENUS SINGAFROTYPA (ARANEAE, ARANEIDAE)

Abstract The African spider genus Singafrotypa Benoit is redescribed and transferred from the tetragnathid subfamily Nephilinae to the araneid subfamily Araneinae. Cladistic analysis of the matrix of Scharff & Coddington (1997) with the addition of two Singafrotypa species supports this new placement. Singafrotypa acanthopus Simon, the type species of the genus, is described along with two new species: Singafrotypa okavango new species from Botswana, and Singafrotypa mandela new species from South Africa. Singafrotypa goliath Benoit is transferred to Neoscona Simon (Araneidae, Araneinae).

Testing ecological and developmental hypotheses of mean and variation in adult size in nephilid orb-weaving spiders

Fecundity selection has been hypothesized to drive the evolution of female gigantism in the orb-weaving family Nephilidae. Several species of these spiders also exhibit large amounts of variation in size at maturity in one or both sexes. In this article, we attempt to detect correlations of mean and variation in adult size at a phylogenetic scale between the sexes and with latitude. We tested six predictions derived from three broad developmental, ecological, and age structure hypotheses, using independent contrasts and a recent species-level nephilid phylogeny as well as least squares and other conventional statistics: 1. In both sexes, species with larger mean size will have greater variation in size; 2. Males and females will show correlated changes in mean size and of variation in size; 3. In both sexes, mean size will be negatively correlated with the midpoint of the latitudinal range; 4. In both sexes, tropical species will be more variable; 5. In both sexes, more widespread species will be more variable; 6. Variation in male size will be positively correlated with mean female size. In no cases were male and female development correlated, suggesting that in this lineage male and female body size evolve independently. The only significant trend detected was a positive phylogenetic correlation between variation in female size and latitude, the opposite of prediction 4. Power tests showed that in all tests of the ecological hypothesis, sample sizes were more than adequate to detect significant trends, if present. Our results suggest that evolutionary trends in juvenile development among species are too weak to be detectable in such data sets.