Incomplete lineage sorting and ancient admixture, and speciation without morphological change in ghost-worm cryptic species

José Cerca; Angel G Rivera-Colón; Mafalda S Ferreira; Mark Ravinet; Michael D Nowak; Julian M Catchen; Torsten H Struck

doi:10.7717/peerj.10896

Incomplete lineage sorting and ancient admixture, and speciation without morphological change in ghost-worm cryptic species

PeerJ. 2021 Feb 9:9:e10896. doi: 10.7717/peerj.10896. eCollection 2021.

Authors

José Cerca^{1

2

3}, Angel G Rivera-Colón⁴, Mafalda S Ferreira^{5

6

7}, Mark Ravinet^{8

9}, Michael D Nowak³, Julian M Catchen⁴, Torsten H Struck³

Affiliations

¹ Department of Environmental Science, Policy, and Management, University of California, University of California, Berkeley, Berkeley, CA, United States of America.
² Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology, Trondheim, Norway.
³ Natural History Museum, University of Oslo, Oslo, Norway.
⁴ Department of Evolution, Ecology, and Behavior, University of Illinois at Urbana-Champaign, Urbana Champaign, IL, United States of America.
⁵ Division of Biological Sciences, University of Montana, Missoula, MT, United States of America.
⁶ Departamento de Biologia, Universidade do Porto, Porto, Porto, Portugal.
⁷ CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Porto, Porto, Portugal.
⁸ School of Life Sciences, University of Nottingham, Nottingham, United Kingdom.
⁹ Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, Norway.

Abstract

Morphologically similar species, that is cryptic species, may be similar or quasi-similar owing to the deceleration of morphological evolution and stasis. While the factors underlying the deceleration of morphological evolution or stasis in cryptic species remain unknown, decades of research in the field of paleontology on punctuated equilibrium have originated clear hypotheses. Species are expected to remain morphologically identical in scenarios of shared genetic variation, such as hybridization and incomplete lineage sorting, or in scenarios where bottlenecks reduce genetic variation and constrain the evolution of morphology. Here, focusing on three morphologically similar Stygocapitella species, we employ a whole-genome amplification method (WGA) coupled with double-digestion restriction-site associated DNA sequencing (ddRAD) to reconstruct the evolutionary history of the species complex. We explore population structure, use population-level statistics to determine the degree of connectivity between populations and species, and determine the most likely demographic scenarios which generally reject for recent hybridization. We find that the combination of WGA and ddRAD allowed us to obtain genomic-level data from microscopic eukaryotes (∼1 millimetre) opening up opportunities for those working with population genomics and phylogenomics in such taxa. The three species share genetic variance, likely from incomplete lineage sorting and ancient admixture. We speculate that the degree of shared variation might underlie morphological similarity in the Atlantic species complex.

Keywords: Genomics; Morphological evolution; Morphology; Phylogenetics; RADseq; Rapid evolution; Sibling species; Slow evolution; Stasis.

Grants and funding

Fieldwork was supported by internal funds, a Den Grevelige Hjelmstjerne-Rosencroneske Stiftelse ved UiO (José Cerca), and THS was supported by the EU Assemble program. A UiO:LifeScience internationalization support and a Godfrey Hewitt mobility award allowed José Cerca to visit Julian Catchen at the UIUC. MSF was supported by POPH-QREN funds from ESF and Portuguese MCTES/FCT (PD/BD/108131/2015 PhD grant in the scope of BIODIV PhD programme at Faculty of Sciences, University of Porto) and NSF (OIA-1736249). There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.