Cryptic ecological and geographic diversification in coral-associated nudibranchs

Highlights

• Comprehensive taxonomic coverage of coral-feeding Tenellia from across the Indo-Pacific.

• Seventeen undescribed species, increasing coral-feeding Tenellia diversity by factor of three.

• Geographic divergence and ecological divergence through host shifting and host specialization.

• Supports ecological speciation as a source of biodiversity on coral reefs.

Abstract

Coral reefs are among the most biologically diverse ecosystems of the world, yet little is known about the processes creating and maintaining their diversity. Ecologically, corallivory in nudibranchs resembles phytophagy in insects- a process that for decades has served as a model for ecological speciation via host shifting. This study uses extensive field collections, DNA sequencing, and phylogenetic analyses to reconstruct the evolutionary history of coral-associated nudibranchs and assess the relative roles that host shifting and geography may have played in their diversification. We find that the number of species is three times higher than the number previously known to science, with evidence for both allopatric and ecological divergence through host shifting and host specialization. Results contribute to growing support for the importance of ecological diversification in marine environments and provide evidence for new species in the genus Tenellia.

Introduction

The relative importance of natural selection and geographic barriers in the process of speciation is one of the most enduring questions in evolutionary biology (Mayr, 1942, Mayr, 1963, Maynard Smith, 1966, Coyne and Orr, 2004). Although allopatric speciation is viewed as the dominant form of speciation (Coyne and Orr, 2004, Smith et al., 2014, Yukilevich, 2014), it is well accepted that natural selection can also drive sympatric speciation in the absence of geographic barriers (Bolnick and Fitzpatrick, 2007, Dieckmann and Doebeli, 1999, Gavrilets, 2014, Schluter, 2001, Thoday and Gibson, 1970). However, the relative importance of natural selection in driving diversification of life on Earth is not well understood, especially in clades of organisms exhibiting trophic diversification as they undergo speciation.

One way that natural selection can drive speciation is when disruptive selection acts on populations occupying different ecological niches and leads to reproductive isolation of those populations. This process, termed “ecological speciation,” has been widely assimilated into the literature as a mechanism for speciation across the tree of life (Rundle and Nosil, 2005, Schluter, 2009). Ecological speciation can happen through a variety of mechanisms, such as obtaining traits that allow for adaptation to distinct trophic niches (Fan et al., 2012, Grant and Grant, 1997, Lu and Bernatchez, 1999), or across environmental gradients (Bird et al., 2011, Lowry et al., 2008, Schneider et al., 1999). Perhaps one of the most common mechanisms for ecological speciation is when selection acts on traits associated with resource use, driving reproductive isolation between populations using different resources (Schluter, 2001).

Many authors propose adaptive resource specialization or resource shifts as important drivers of diversification in large taxonomic groups such as fish (Burress, 2014, Litsios et al., 2012), crustaceans (Hurt et al., 2013, Malay and Michonneau, 2014), mollusks (Krug, 2011, Wägele, 2004), and insects (Kjellberg and Proffit, 2016, Nyman et al., 2007). There are numerous examples of phytophagous insects that have undergone ecological speciation by shifting to novel host plants (Berlocher and Feder, 2002, Hébert et al., 2016).

Like plants, scleractinian corals play host to a variety of taxa. The diversity of coral symbionts includes algae, crabs, barnacles, polychaete worms, and gastropods (Faucci et al., 2007, Malay and Michonneau, 2014, McKeon et al., 2012, Parkinson et al., 2016, Tsang et al., 2009, Willette et al., 2015). The obligate relationship between these organisms and their coral hosts (Hadfield and Pennington, 1990) draws a strong parallel to phytophagous insects and plants. Given that phytophagous insects and plants are a model system for understanding ecological speciation through host shifting, similar processes could drive speciation in coral-associated taxa as well. However, research on ecological speciation on coral reefs lags far behind that in terrestrial and aquatic systems (Miglietta et al., 2011, Rocha et al., 2005). Instead, most studies still seek allopatric explanations for species diversity, even when there are presently no obvious geographic barriers to promote divergence (Barber et al., 2006, Briggs, 2005). As a result, we still have an incomplete understanding of species diversification processes in the marine environment, particularly within biodiversity hotspots like the Coral Triangle, the world’s most biodiverse marine ecosystem (Roberts et al., 2002).

Aeolid nudibranchs are an extremely species rich group of sea slugs known for diversification and specialization on cnidarian prey (Carmona et al., 2013, McDonald and Nybakken, 1997). While most aeolids specialize on hydroids or anemones, some are known to live and feed on specific genera or species of scleractinian corals (Faucci et al., 2007, Rudman, 1981, Rudman, 1982). Planktonic nudibranch larvae settle and metamorphose on their preferred host coral species (or genus) in response to chemical cues produced by that coral (Hadfield and Pennington, 1990). Moreover, individual nudibranchs typically stay on one host colony for their entire adult life, including mating, because adults have limited mobility and host coral colonies are large enough to accommodate several nudibranchs (Krug, 2011). This uncommon life-history could promote reproductive isolation between populations that feed on different coral species, potentially leading to ecological speciation as demonstrated in corallivorous snails (Simmonds et al. 2018).

Scleractinian corallivory has been reported in nine species of aeolids: Pinufius rebus, Tenellia poritophages (previously Cuthona), and seven Tenellia species that were previously known as Phestilla, three of which are yet undescribed (Faucci et al., 2007, Gosliner et al., 2015, Wong et al., 2017). Recent work suggests that all scleractinian-feeding aeolids belong to one clade, implying that this feeding behavior has only evolved once (Cella et al., 2016). Within the Phestilla clade of Tenellia, host shifting from one group of corals to another has occurred at least twice (Faucci et al., 2007), suggesting that diversification in this group could be driven by ecological speciation. However, incomplete understanding of the taxonomy and phylogenetic relationships in this group precludes systematic tests of speciation processes.

This study reconstructs the evolutionary history of all scleractinian-feeding nudibranchs to assess the relative roles that host shifting and geography may have played in lineage diversification. Toward these aims we a) conducted exploratory field sampling to discover species with previously unknown host associations, b) used DNA sequencing to detect cryptic species, and c) built a phylogenetic tree of all scleractinian-associated nudibranchs to determine how frequently and where host shifting has occurred throughout their evolutionary history.