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Systematics, Toxins, Parasitoids, and Niche: an Integrative Approach to the Study of a New Black Widow Spider in Colombia

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Systematics, Toxins, Parasitoids, and Niche: an Integrative Approach to the Study of a New Black Widow Spider in Colombia SYSTEMATICS, TOXINS, PARASITOIDS, AND NICHE: AN INTEGRATIVE APPROACH TO THE STUDY OF A NEW BLACK WIDOW SPIDER IN COLOMBIA Doctoral Thesis presented by: Martha Alexandra Rueda Esteban Advisor: Emilio Realpe PhD. Co-Advisor: Adolfo Amézquita PhD. Evaluator: Charles Griswold Evaluator: Jorge Molina Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor in Philosophy Department of Biological Sciences Graduate School Universidad de los Andes Bogotá, Colombia. 2018 1 Abstract Black widow spiders have been widely studied because they are medically important due to the syndrome produced after a bite. The syndrome can produce local or systemic reactions and can be fatal. Also, because of the difficulty in their classification; the color pattern polymorphism, and the similarities in the reproductive systems have been a problem in the differentiation and taxonomic identification of species by morphology. There are 31 species of Latrodectus described worldwide, and two species described for Colombia, L. curacaviensis (Müller, 1776) and L. geometricus Koch, 1841. L. geometricus is the only cosmopolitan species and has been classified as invasive in many ecosystems; this species origin is not known yet, but the closest phylogenetic relative is from Africa. L. curacaviensis was recognized as a species after many changes in its classification. This species was last reported in Colombia in the department of Atlantico, north of the country. Black widows in Colombia are known since 1538, when Gonzalo Jimenez de Quesada reported deaths in his army by the bite of a deadly red spider in the “Valley of sadness”, the Tatacoa desert, southwestern Colombia. This unknown species has been described in many natural history essays and medical articles in Colombia since that date, but they refer to the spider with the common Latin-American black widow name “coya”; there is no reference to a specific species and the knowledge of the epidemiological problem this unknown species impose, is null. According to previous studies, L. geometricus and L. curacaviensis have a Lethal Dose 50 of 22.5 mg/kg and 12 mg/kg respectively, and the amount of dry venom injected in Latrodectus spiders ranges between 0.02-0.03 mg; showing that none of these two species can produce the symptoms described in the natural history essays and medical articles from the Tatacoa desert. The first chapter in this Thesis studies the medical 2 importance of the unidentified species from the Tatacoa desert, in order to determine if that morphotype has the presence of the α-latrotoxin and can be the species reported in all the previous reports of Latrodetism in the Country. The toxin was found in the venom of the Latrodectus species found in the Tatacoa desert and the symptoms observed were consistent with the symptoms described for the syndrome. Therefore, the species present in the Tatacoa desert do not belong to any of the species described for the Country and a study of the identity of the species, ecology, taxonomy, or evolution of this genus in the Country is needed. The second chapter identifies the Tatacoa spider as a new Latrodectus species, and describes a different morphotype in Santander, also classified as a new species. New population reports for 10 departments in the country are made for L. geometricus and L. curacaviensis. Also, a synonymy for two South-American species, described originally in Argentina, is determined. The species report is made by morphological and molecular data; based in the analysis of partial sequences of the mitochondrial cytochrome c oxidase subunit I (COI), and the mitochondrial ribosomal RNA gene 16S (16SrRNA), including a phylogenetic and genetic analysis, that show enough support for the new species status. One candidate species is described for Santander department, this species shows a close genetic relation to L. hesperus Chamberlin and Ivie, 1935, and the same color pattern change during ontogeny. The Tatacoa desert candidate species is described for Huila and Tolima departments, and show a highly close genetic relation to L. corallinus Abalos, 1980 and L. diaguita Carcavallo, 1960; also, the genetic analyses show enough similarity between L. corallinus and L. diaguita to support the synonymy between these two species. The Colombian population of the Tatacoa candidate species was found apparently co- existing with L. geometricus in the “desert”, until 2016 when it disappeared from the ecosystem and is presumed to be locally extinct. 3 This local extinction raises the question about the possible co-existence, competition, and segregation of these two species in this community. The third chapter studies the two sympatric populations in the Tatacoa desert, and the possible variables that acted as ecological pressure in the local extinction of Latrodectus sp. The niche width was measured using several environmental and trophic variables to determine the overlap and evaluate the differences that allowed them to share the ecosystem for so many years. The trophic variables used included dry cocoons of prey found in the webs analyzed by direct observation, and metagenomic data from gut content analysis. The environmental and trophic niche breadth of L. geometricus were bigger than the niche of Latrodectus sp. and a complete overlap was observed. After 2016, Latrodectus sp. was not found in the desert and a local extinction was declared. More populations of this species were found north of the desert, in dry and warm places where L. geometricus has not stablished yet. A case of competition between two species is described, but the co-existence in a community is not only reduced to the inter-specific relations with just one species, ecological pressure given by predation and parasitism can also have influence in the population density of a species. Chapter four aims to expand the ecological analysis of co-existence and evaluate parasitoidism to determine if that could have been acting as ecological pressure and be one of the explanations to the local extinction of Latrodectus sp. in the Tatacoa desert. Two species of parasitoids were found in the egg sacs of both spider species while co-existing. Ecological variables were measured and habitat preference by the parasitoids was found. Also, number of healthy egg sacs and egg sacs with the presence of parasitoids by each species was determined. The sample number did not allow to evaluate host preference. 4 Dedication To my mentor and dear friend Emilio Realpe for teaching me the love for arthropods. To my co-advisor and guide Adolfo Amézquita. To LAZOEA for all the support and help all these years. To my family and friends, for being patient enough to survive the Ph.D. with me. 5 Contents Abstract ......................................................................................................................................... 2 Dedication ..................................................................................................................................... 5 General Introduction .................................................................................................................. 8 General Introduction References .................................................................................. 18 General Introduction Figure Legends ........................................................................... 27 General Introduction Figures ....................................................................................... 28 Chapter 1: Toxicity evaluation and initial characterization of the venom of a Colombian Latrodectus sp. ............................................................................................................................ 30 Chapter 1 References ................................................................................................... 44 Chapter 1 Figure Legends ............................................................................................ 49 Chapter 1 Table Legends .............................................................................................. 50 Chapter 1 Figures ......................................................................................................... 51 Chapter 1 Tables........................................................................................................... 53 Chapter 2: Two new species of Latrodectus (Araneae: Theridiidae) from the dry forests in the Magdalena Valley, Colombia ............................................................................................. 55 Chapter 2 References ................................................................................................... 74 Chapter 2 Figure Legends ............................................................................................ 78 Chapter 2 Figures ......................................................................................................... 80 Supplementary Material Files: Chapter 2 ..................................................................... 88 Chapter 3: Niche overlap in two sympatric species of black widows in Colombia using ecological and genomic data ................................................................................................... 111 Chapter 3 References ................................................................................................. 131 Chapter 3 Figure Legends .......................................................................................... 138 Chapter 3 Table Legends ...........................................................................................
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