Ecological speciation by sympatric host shifts in a clade of herbivorous sea slugs, with introgression and localized mitochondrial capture between species

Host shifting in insect-plant systems was historically important to the
development of ecological speciation theory, yet surprisingly few studies
have examined whether host shifting drives the diversification of marine
herbivores. When small-bodied consumers feed and also mate on a preferred
host, disruptive selection can split a population into host races despite
gene flow. Support for host shifts is notably lacking for invertebrates
associated with macroalgae, where the scale of dispersal by planktonic
larvae often far exceeds the grain of host patchiness, and adults are
typically less specialized than terrestrial herbivores. Here, we present a
candidate example of ecological speciation in a clade of sea slugs that
primarily consume green algae in the genus Caulerpa, including highly
invasive species. Ancestral character state reconstructions supported ‘sea
grapes’ (C. racemosa, C. lentillifera) as the ancestral host for a
tropical radiation of 12 Elysia spp., with one shift onto alternative
Caulerpa spp. in the Indo-Pacific. A Caribbean radiation of three species
included symaptric host shifts to Rhipocephalus brevicaulis in the
ancestor of E. pratensis Ortea & Espinosa, 1996, and to C.
prolifera in E. hamanni Krug, Vendetti & Valdes 2016, plus a niche
expansion to a range of Caulerpa spp. in E. subornata Verrill, 1901. All
three species are broadly sympatric across the Caribbean but are
host-partitioned at a fine grain, and distinct by morphology and at
nuclear loci. However, non-recombining mtDNA revealed a history of gene
flow between E. pratensis and E. subornata: COI haplotypes from E.
subornata were 10.4% divergent from E. pratensis haplotypes from four
sites, but closely related to all E. pratensis haplotypes sampled from six
Bahamian islands, indicating historical introgression and localized
“mitochondrial capture.” Disruptive selective likely fueled divergence and
adaptation to distinct host environments, indicating ecological speciation
may be an under-appreciated driver of diversification for marine
herbivores as well as epibionts and other resource specialists.