Understanding Species Boundaries that Arise from Complex Histories: Gene Flow Across the Speciation Continuum in the Spotted Whiptail Lizards

Author:

Barley Anthony J1ORCID,Nieto-Montes de Oca Adrián2,Manríquez-Morán Norma L3,Thomson Robert C4ORCID

Affiliation:

1. School of Mathematical and Natural Sciences, Arizona State University, West Valley Campus , 4701 W Thunderbird Road, Glendale, AZ 85306 , USA

2. Laboratorio de Herpetología and Museo de Zoología Alfonso L. Herrera, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Cd. Universitaria, Del. Coyoacán , Ciudad de México, C.P. 04510 , México

3. Laboratorio de Sistemática Molecular, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Km. 4.5 Carr. Pachuca-Tulancingo, Col. Carboneras, Mineral de la Reforma, Hidalgo , C.P. 42184 ,  México

4. School of Life Sciences, University of Hawai’i , 3190 Maile Way, Honolulu, HI 96822 , USA

Abstract

Abstract Gene flow between diverging lineages challenges the resolution of species boundaries and the understanding of evolutionary history in recent radiations. Here, we integrate phylogenetic and coalescent tools to resolve reticulate patterns of diversification and use a perspective focused on evolutionary mechanisms to distinguish interspecific and intraspecific taxonomic variation. We use this approach to resolve the systematics for one of the most intensively studied but difficult to understand groups of reptiles: the spotted whiptail lizards of the genus Aspidoscelis (A. gularis complex). Whiptails contain the largest number of unisexual species known within any vertebrate group and the spotted whiptail complex has played a key role in the generation of this diversity through hybrid speciation. Understanding lineage boundaries and the evolutionary history of divergence and reticulation within this group is therefore key to understanding the generation of unisexual diversity in whiptails. Despite this importance, long-standing confusion about their systematics has impeded understanding of which gonochoristic species have contributed to the formation of unisexual lineages. Using reduced representation genomic data, we resolve patterns of divergence and gene flow within the spotted whiptails and clarify patterns of hybrid speciation. We find evidence that biogeographically structured ecological and environmental variation has been important in morphological and genetic diversification, as well as the maintenance of species boundaries in this system. Our study elucidates how gene flow among lineages and the continuous nature of speciation can bias the practice of species delimitation and lead taxonomists operating under different frameworks to different conclusions (here we propose that a 2 species arrangement best reflects our current understanding). In doing so, this study provides conceptual and methodological insights into approaches to resolving diversification patterns and species boundaries in rapid radiations with complex histories, as well as long-standing taxonomic challenges in the field of systematic biology.

Publisher

Oxford University Press (OUP)

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