The Base of the Animal Tree?: The identity of the most basal lineages of the animal kingdom evolutionary tree has long been contested. Ryan et al. (p. 10.1126/science.1242592 ; see the Perspective by Rokas ) sequenced the genome of the ctenophore the warty comb jelly or sea walnut, Mnemiopsis leidyi , and conclude that ctenophores alone, not sponges or the clade consisting of both ctenophores and cnidarians, are the most basal extant animals. The results suggest a specific evolutionary process that likely occurred—including repeated gains and loss of mesoderm, expansion of genes associated with the cell cycle, growth signaling, apoptosis, and epithelial and neural cell types. Furthermore, previous hypotheses regarding the evolution of animals may require re-evaluation.

Sponges and evolutionary origins: Sponges represent our distant animal relatives. They do not have a nervous system but do have a simple body for filter feeding. Surveying the cell types in the freshwater sponge Spongilla lacustris , Musser et al . found that many genes important in synaptic communication are expressed in cells of the small digestive chambers. They found secretory machinery characteristic of the presynapse in small multipolar cells contacting all other cells and also the receptive apparatus of the postsynapse in the choanocytes that generate water flow and digest microbial food. These results suggest that the first directed communication in animals may have evolved to regulate feeding, serving as a starting point on the long path toward nervous system evolution. —BAP

The genomes of non-bilaterian metazoans are key to understanding the molecular basis of early animal evolution. However, a full comprehension of how animal-specific traits, such as nervous systems, arose is hindered by the scarcity and fragmented nature of genomes from key taxa, such as Porifera. Ephydatia muelleri is a freshwater sponge found across the northern hemisphere. Here, we present its 326 Mb genome, assembled to high contiguity (N50: 9.88 Mb) with 23 chromosomes on 24 scaffolds. Our analyses reveal a metazoan-typical genome architecture, with highly shared synteny across Metazoa, and suggest that adaptation to the extreme temperatures and conditions found in freshwater often involves gene duplication. The pancontinental distribution and ready laboratory culture of E. muelleri make this a highly practical model system which, with RNAseq, DNA methylation and bacterial amplicon data spanning its development and range, allows exploration of genomic changes both within sponges and in early animal evolution.

Animals have a carefully orchestrated relationship with oxygen. When exposed to low environmental oxygen concentrations, and during periods of increased energy expenditure, animals maintain cellular oxygen homeostasis by enhancing internal oxygen delivery, and by enabling the anaerobic production of ATP. These low-oxygen responses are thought to be controlled universally across animals by the hypoxia-inducible factor (HIF). We find, however, that sponge and ctenophore genomes lack key components of the HIF pathway. Since sponges and ctenophores are likely sister to all remaining animal phyla, the last common ancestor of extant animals likely lacked the HIF pathway as well. Laboratory experiments show that the marine sponge Tethya wilhelma maintains normal transcription under oxygen levels down to 0.25% of modern atmospheric saturation, the lowest levels we investigated, consistent with the predicted absence of HIF or any other HIF-like pathway. Thus, the last common ancestor of all living animals could have metabolized aerobically under very low environmental oxygen concentrations.

Placozoans are a phylum of nonbilaterian marine animals currently represented by a single described species, Trichoplax adhaerens, Schulze 1883. Placozoans arguably show the simplest animal morphology, which is identical among isolates collected worldwide, despite an apparently sizeable genetic diversity within the phylum. Here, we use a comparative genomics approach for a deeper appreciation of the structure and causes of the deeply diverging lineages in the Placozoa. We generated a high-quality draft genome of the genetic lineage H13 isolated from Hong Kong and compared it to the distantly related T. adhaerens. We uncovered substantial structural differences between the two genomes that point to a deep genomic separation and provide support that adaptation by gene duplication is likely a crucial mechanism in placozoan speciation. We further provide genetic evidence for reproductively isolated species and suggest a genus-level difference of H13 to T. adhaerens, justifying the designation of H13 as a new species, Hoilungia hongkongensis nov. gen., nov. spec., now the second described placozoan species and the first in a new genus. Our multilevel comparative genomics approach is, therefore, likely to prove valuable for species distinctions in other cryptic microscopic animal groups that lack diagnostic morphological characters, such as some nematodes, copepods, rotifers, or mites. Placozoans are a phylum of tiny (approximately 1 mm) marine animals that are found worldwide in temperate and tropical waters. They are characterized by morphological simplicity, with only a handful of cell types, no neurons, no tissue organization, and even no axial polarity. Since the original description of Trichoplax adhaerens 135 years ago, no additional accepted species has been established, leaving the Placozoa as the only animal phylum with only a single formally described species. While classical morphological species identification has failed to reveal further species, single-gene DNA sequence analyses have identified a broad and deep genetic diversity within the Placozoa. To address the significance of this deep genetic diversity in this morphologically uniform phylum, and to better understand its consequences for speciation processes, general biology, and species delimitation in the Placozoa, we sequenced the genome of the placozoan isolate “H13,” a lineage distantly genetically related to T. adhaerens. Our multilevel genomic comparisons with the T. adhaerens genome show considerable differences in the general structure of the genome and the makeup and history of various gene families of biological relevance to habitat adaptation. Based on comparative genomics, we here describe the second placozoan species and show that it belongs to a new genus.