A molecular phylogeny of nephilid spiders: evolutionary history of a model lineage
- PMID:23811436
- DOI: 10.1016/j.ympev.2013.06.008
A molecular phylogeny of nephilid spiders: evolutionary history of a model lineage
Abstract
The pantropical orb web spider family Nephilidae is known for the most extreme sexual size dimorphism among terrestrial animals. Numerous studies have made Nephilidae, particularly Nephila, a model lineage in evolutionary research. However, a poorly understood phylogeny of this lineage, relying only on morphology, has prevented thorough evolutionary syntheses of nephilid biology. We here use three nuclear and five mitochondrial genes for 28 out of 40 nephilid species to provide a more robust nephilid phylogeny and infer clade ages in a fossil-calibrated Bayesian framework. We complement the molecular analyses with total evidence analysis including morphology. All analyses find strong support for nephilid monophyly and exclusivity and the monophyly of the genera Herennia and Clitaetra. The inferred phylogenetic structure within Nephilidae is novel and conflicts with morphological phylogeny and traditional taxonomy. Nephilengys species fall into two clades, one with Australasian species (true Nephilengys) as sister to Herennia, and another with Afrotropical species (Nephilingis Kuntner new genus) as sister to a clade containing Clitaetra plus most currently described Nephila. Surprisingly, Nephila is also diphyletic, with true Nephila containing N. pilipes+N. constricta, and the second clade with all other species sister to Clitaetra; this "Nephila" clade is further split into an Australasian clade that also contains the South American N. sexpunctata and the Eurasian N. clavata, and an African clade that also contains the Panamerican N. clavipes. An approximately unbiased test constraining the monophyly of Nephilengys, Nephila, and Nephilinae (Nephila, Nephilengys, Herennia), respectively, rejected Nephilengys monophyly, but not that of Nephila and Nephilinae. Further data are therefore necessary to robustly test these two new, but inconclusive findings, and also to further test the precise placement of Nephilidae within the Araneoidea. For divergence date estimation we set the minimum bound for the stems of Nephilidae at 40 Ma and of Nephila at 16 Ma to accommodate Palaeonephila from Baltic amber and Dominican Nephila species, respectively. We also calibrated and dated the phylogeny under three different interpretations of the enigmatic 165 Ma fossil Nephila jurassica, which we suspected based on morphology to be misplaced. We found that by treating N. jurassica as stem Nephila or nephilid the inferred clade ages were vastly older, and the mitochondrial substitution rates much slower than expected from other empirical spider data. This suggests that N. jurassica is not a Nephila nor a nephilid, but possibly a stem orbicularian. The estimated nephilid ancestral age (40-60 Ma) rejects a Gondwanan origin of the family as most of the southern continents were already split at that time. The origin of the family is equally likely to be African, Asian, or Australasian, with a global biogeographic history dominated by dispersal events. A reinterpretation of web architecture evolution suggests that a partially arboricolous, asymmetric orb web with a retreat, as exemplified by both groups of "Nephilengys", is plesiomorphic in Nephilidae, that this architecture was modified into specialized arboricolous webs in Herennia and independently in Clitaetra, and that the web became aerial, gigantic, and golden independently in both "Nephila" groups. The new topology questions previously hypothesized gradual evolution of female size from small to large, and rather suggests a more mosaic evolutionary pattern with independent female size increases from medium to giant in both "Nephila" clades, and two reversals back to medium and small; combined with male size evolution, this pattern will help detect gross evolutionary events leading to extreme sexual size dimorphism, and its morphological and behavioral correlates.
Keywords: Biogeography; Coevolution; Female gigantism; Nephila; Sexual selection; Sexual size dimorphism.
Copyright © 2013 Elsevier Inc. All rights reserved.
Similar articles
- Golden Orbweavers Ignore Biological Rules: Phylogenomic and Comparative Analyses Unravel a Complex Evolution of Sexual Size Dimorphism.Kuntner M, Hamilton CA, Cheng RC, Gregorič M, Lupše N, Lokovšek T, Lemmon EM, Lemmon AR, Agnarsson I, Coddington JA, Bond JE.Kuntner M, et al.Syst Biol. 2019 Jul 1;68(4):555-572. doi: 10.1093/sysbio/syy082.Syst Biol. 2019.PMID:30517732Free PMC article.
- Biogeography and speciation patterns of the golden orb spider genus Nephila (Araneae: Nephilidae) in Asia.Su YC, Chang YH, Smith D, Zhu MS, Kuntner M, Tso IM.Su YC, et al.Zoolog Sci. 2011 Jan;28(1):47-55. doi: 10.2108/zsj.28.47.Zoolog Sci. 2011.PMID:21186947
- Biogeography and diversification of hermit spiders on Indian Ocean islands (Nephilidae: Nephilengys).Kuntner M, Agnarsson I.Kuntner M, et al.Mol Phylogenet Evol. 2011 May;59(2):477-88. doi: 10.1016/j.ympev.2011.02.002. Epub 2011 Feb 21.Mol Phylogenet Evol. 2011.PMID:21316478
- Systematics, phylogeny, and evolution of orb-weaving spiders.Hormiga G, Griswold CE.Hormiga G, et al.Annu Rev Entomol. 2014;59:487-512. doi: 10.1146/annurev-ento-011613-162046. Epub 2013 Oct 25.Annu Rev Entomol. 2014.PMID:24160416Review.
- Sexual Size Dimorphism: Evolution and Perils of Extreme Phenotypes in Spiders.Kuntner M, Coddington JA.Kuntner M, et al.Annu Rev Entomol. 2020 Jan 7;65:57-80. doi: 10.1146/annurev-ento-011019-025032. Epub 2019 Oct 1.Annu Rev Entomol. 2020.PMID:31573828Review.
Cited by
- Phylogeny predicts future habitat shifts due to climate change.Kuntner M, Năpăruş M, Li D, Coddington JA.Kuntner M, et al.PLoS One. 2014 Jun 3;9(6):e98907. doi: 10.1371/journal.pone.0098907. eCollection 2014.PLoS One. 2014.PMID:24892737Free PMC article.
- Potential costs of heterospecific sexual interactions in golden orbweb spiders (Nephila spp.).Quiñones-Lebrón SG, Kralj-Fišer S, Gregorič M, Lokovšek T, Čandek K, Haddad CR, Kuntner M.Quiñones-Lebrón SG, et al.Sci Rep. 2016 Nov 15;6:36908. doi: 10.1038/srep36908.Sci Rep. 2016.PMID:27845369Free PMC article.
- Nephila clavata L Koch, the Joro Spider of East Asia, newly recorded from North America (Araneae: Nephilidae).Hoebeke ER, Huffmaster W, Freeman BJ.Hoebeke ER, et al.PeerJ. 2015 Feb 5;3:e763. doi: 10.7717/peerj.763. eCollection 2015.PeerJ. 2015.PMID:25699210Free PMC article.
- Coevolution of female and male genital components to avoid genital size mismatches in sexually dimorphic spiders.Lupše N, Cheng RC, Kuntner M.Lupše N, et al.BMC Evol Biol. 2016 Aug 17;16(1):161. doi: 10.1186/s12862-016-0734-9.BMC Evol Biol. 2016.PMID:27535025Free PMC article.
- Increasing Information Content and Diagnosability in Family-Level Classifications.Kuntner M, Čandek K, Gregorič M, Turk E, Hamilton CA, Chamberland L, Starrett J, Cheng RC, Coddington JA, Agnarsson I, Bond JE.Kuntner M, et al.Syst Biol. 2023 Aug 7;72(4):964-971. doi: 10.1093/sysbio/syad021.Syst Biol. 2023.PMID:37161751Free PMC article.
Publication types
MeSH terms
Substances
Related information
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases