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ABSTRACT Many coastal marine species experienced Pleistocene gene flow between the North Pacific and Atlantic. Understanding historical connectivity between ocean basins should aid in predicting how regional faunas will respond to recent warming that has intensified trans‐Arctic dispersal. Wetland fauna of the Northwestern Atlantic may have survived in estuarine refugia throughout glacial cycles, or recolonised from the southern coast, North Pacific or Northeastern Atlantic. Here, we used multilocus genetic markers and historical climate data to investigate lineage distribution and connectivity among populations of the nominally cosmopolitan sea slugAlderia modesta, sampled from mudflats on both coasts of the North Pacific and North Atlantic. Mitochondrial DNA clades from European and North American populations were deeply divergent and reciprocally monophyletic; differences at seven polymorphic nuclear loci indicated prolonged absence of trans‐Atlantic gene flow. A Pacific ancestor likely first colonised the Atlantic during the marine biotic interchange of the middle Pliocene ~3.5 Ma. Both mtDNA phylogenetics and nuclear genotype assignments support repeated trans‐Arctic colonisation of the Northwestern Atlantic from the Pacific during inter‐glacial cycles; no gene flow was evident since the last glacial maximum, however. Time‐calibrated coalescent phylogenies, Bayesian skyline plots and haplotype networks all indicated recent population expansions in the Pacific and Europe, but not Northwestern Atlantic. In both the Pacific and Northwestern Atlantic, older lineages persisted in patchy refugia north of glacial margins, while a derived clade of Pacific haplotypes indicates northward post‐LGM expansion. The biogeographical history ofAlderiacontrasts with rocky‐shore taxa that were largely extirpated by glacial advance and recolonised from refugia following the last glacial maximum. Based on molecular differences and distinctions in radular and penial stylet morphology, we resurrect the nameAlderia harvardiensisGould 1870 forAlderiafrom the Northwestern Atlantic and North Pacific;A. modestarefers exclusively to European slugs. 

Secondary metabolites often function as antipredator defenses, but when bioactive at low concentrations, their off-target effects on other organisms may be overlooked. Candidate “keystone molecules” are proposed to affect community structure and ecosystem functions, generally originating as defenses of primary producers; the broader effects of animal chemistry remain largely unexplored, however. Here, we characterize five previously unreported polyketides (alderenes A to E) biosynthesized by sea slugs reaching exceptional densities (up to 9000 slugs per square meter) in Northern Hemisphere estuaries. Alderenes comprise only 0.1% of slug wet weight, yet rendered live slugs or dead flesh unpalatable to three co-occurring consumers, making a potential food resource unavailable and redirecting energy flow in critical nursery habitat. Alderenes also displaced infauna from the upper sediment of the mudflat but attracted ovipositing snails. By altering communities, such compounds may have unexpected cascading effects on processes ranging from bioturbation to reproduction of species not obviously connected to the producing organisms, warranting greater attention by ecologists. 

Abstract Animals synthesize simple lipids using a distinct fatty acid synthase (FAS) related to the type I polyketide synthase (PKS) enzymes that produce complex specialized metabolites. The evolutionary origin of the animal FAS and its relationship to the diversity of PKSs remain unclear despite the critical role of lipid synthesis in cellular metabolism. Recently, an animal FAS-like PKS (AFPK) was identified in sacoglossan molluscs. Here, we explore the phylogenetic distribution of AFPKs and other PKS and FAS enzymes across the tree of life. We found AFPKs widely distributed in arthropods and molluscs (>6300 newly described AFPK sequences). The AFPKs form a clade with the animal FAS, providing an evolutionary link bridging the type I PKSs and the animal FAS. We found molluscan AFPK diversification correlated with shell loss, suggesting AFPKs provide a chemical defense. Arthropods have few or no PKSs, but our results indicate AFPKs contributed to their ecological and evolutionary success by facilitating branched hydrocarbon and pheromone biosynthesis. Although animal metabolism is well studied, surprising new metabolic enzyme classes such as AFPKs await discovery. 

Animal cytoplasmic fatty acid synthase (FAS) represents a unique family of enzymes that are classically thought to be most closely related to fungal polyketide synthase (PKS). Recently, a widespread family of animal lipid metabolic enzymes has been described that bridges the gap between these two ubiquitous and important enzyme classes: the animal FAS–like PKSs (AFPKs). Although very similar in sequence to FAS enzymes that produce saturated lipids widely found in animals, AFPKs instead produce structurally diverse compounds that resemble bioactive polyketides. Little is known about the factors that bridge lipid and polyketide synthesis in the animals. Here, we describe the function of EcPKS2 fromElysia chlorotica, which synthesizes a complex polypropionate natural product found in this mollusc. EcPKS2 starter unit promiscuity potentially explains the high diversity of polyketides found in and among molluscan species. Biochemical comparison of EcPKS2 with the previously described EcPKS1 reveals molecular principles governing substrate selectivity that should apply to related enzymes encoded within the genomes of photosynthetic gastropods. Hybridization experiments combining EcPKS1 and EcPKS2 demonstrate the interactions between the ketoreductase and ketosynthase domains in governing the product outcomes. Overall, these findings enable an understanding of the molecular principles of structural diversity underlying the many molluscan polyketides likely produced by the diverse AFPK enzyme family.