An inordinate fondness for slugs: Phylogenomics of the diverse gastropod clade Heterobranchia, a group key to our understanding of the evolution of shell reduction and loss

• Main Author: Knutson, Vanessa L.
• Other Authors: Girguis, Peter, Srivastava, Mansi, Knoll, Andrew, Davis, Charles
• Format: Thesis
• Language: English
• Published: 2022
• Subjects: heterobranch; phylogenetics; phylotranscriptomics; sea slug; snail; systematics; Biology; Zoology; Evolution & development; Lopez; Medina; Ocean acidification
• Online Access: https://nrs.harvard.edu/URN-3:HUL.INSTREPOS:37371199

Gastropods are exquisitely successful organisms, their shell undoubtedly playing a key role in their success. Despite being such an effective defense mechanism, the gastropod shell has been reduced, lost or internalized several times throughout evolutionary history, occurring in at least four of the six major extant gastropod clades. Most of these “limacization” events are found in the most disparate gastropod subclass, Heterobranchia, a wellspring of fascinating features and behaviors including uptake, storage, and defensive use of stinging cells (Goodheart and Bely, 2017; Greenwood, 2009) (nudibranchs), storage and use of photosynthesizing chloroplasts (Cruz et al., 2020; Hinde and Smith, 1974; Kawaguti and Yamasu, 1965) (sacoglossans), extreme body autotomy and regeneration (sacoglossans) (Mitoh and Yusa, 2021), ocean acidification models (pteropods) (Bednaršek et al., 2012, 2019), disease vectors (Adema et al., 2012; Adenowo et al., 2015), invasive species (Gołdyn et al., 2017) and agricultural/horticultural pests (Laznik et al., 2020) (pulmonate snails), neuroscience and behavior models (Bédécarrats et al., 2018; Conte et al., 2017; Kandel, 2001) (sea hares), and evolutionary transitions into freshwater and terrestrial environments (Holznagel et al., 2010; Jörger et al., 2014; Kano et al., 2015). Despite much research focused on their systematics (Dinapoli and Klussmann-Kolb, 2010; Jörger et al., 2010; Dayrat et al., 2011; Medina et al., 2011; Kocot et al., 2013; Kano et al., 2016; Varney et al., 2021), basic understanding of the evolutionary relationships among several heterobranch lineages has remained elusive, particularly within the paraphyletic assemblage of mostly shelled species known as ‘lower’ Heterobranchia and panpulmonates. To tackle this long-standing gap in systematic knowledge, in Chapter 1, I sequenced and assembled de novo an extensive dataset of heterobranch transcriptomes and used these to perform several phylogenomic analyses of the clade Heterobranchia. Incorporating these data with an exploration of the potential effects of phylogenetic biases (Lopez et al., 2002; Foster, 2004; Degnan and Rosenberg, 2009) and inference methods, I have successfully resolved the relationships among the informal grouping known as ‘lower’ Heterobranchia, discovering a sister group relationship between the families Architectonicidae and Omalogyridae, which together constitute the sister group to the rest of the heterobranchs. My analyses also shed light on remaining unresolved relationships among eupulmonates—the group that includes most of the terrestrial and many freshwater snails and slugs. To better understand the timing of evolution in the group and the sensitivity of selection of calibration points, I produced two time-calibrated phylogenies and explored the effect of including the oldest known—and controversially assigned—valvatoid fossil on heterobranch divergence dates. Additionally, by using a Ks approach, I explored the possibility that ancient whole genome duplications may be present in certain heterobranch clades. Finally, transcriptomic data has the ability to not only resolve the deepest nodes within heterobranchs, but also finer scale relationships within the orders. In Chapter 2, I demonstrate the ability of transcriptomes to provide a phylogenetic backbone to the heterobranch order Cephalaspidea, a group that can provide much insight in the evolution of shell reduction, internalization and loss.