How Did Seal Lice Turn into the Only Truly Marine Insects?

Insects are the most evolutionarily and ecologically successful group of living animals, being present in almost all possible mainland habitats; however, they are virtually absent in the ocean, which constitutes more than 99% of the Earth’s biosphere. Only a few insect species can be found in the sea but they remain at the surface, in salt marshes, estuaries, or shallow waters. Remarkably, a group of 13 species manages to endure long immersion periods in the open sea, as well as deep dives, i.e., seal lice. Sucking lice (Phthiraptera: Anoplura) are ectoparasites of mammals, living while attached to the hosts’ skin, into their fur, or among their hairs. Among them, the family Echinophthiriidae is peculiar because it infests amphibious hosts, such as pinnipeds and otters, who make deep dives and spend from weeks to months in the open sea. During the evolutionary transition of pinnipeds from land to the ocean, echinophthiriid lice had to manage the gradual change to an amphibian lifestyle along with their hosts, some of which may spend more than 80% of the time submerged and performing extreme dives, some beyond 2000 m under the surface. These obligate and permanent ectoparasites have adapted to cope with hypoxia, high salinity, low temperature, and, in particular, conditions of huge hydrostatic pressures. We will discuss some of these adaptations allowing seal lice to cope with their hosts’ amphibious habits and how they can help us understand why insects are so rare in the ocean.

hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea

The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of Hox5/6, -9, -10, and -11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of Hox-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (Leucoraja erinacea). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of hox5/6, hox9, hox10, and hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that hox-based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.

Life History and the Transitions to Eusociality in the Hymenoptera

Although indirect selection through relatives (kin selection) can explain the evolution of effectively sterile offspring that act as helpers at the nest (eusociality) in the ants, bees, and stinging wasps (aculeate Hymenoptera), the genetic, ecological, and life history conditions that favor transitions to eusociality are poorly understood. In this study, ancestral state reconstruction on recently published phylogenies was used to identify the independent transitions to eusociality in each of the taxonomic families that exhibit eusociality. Semisociality, in which a single nest co-foundress monopolizes reproduction, often precedes eusociality outside the vespid wasps. Such a route to eusociality, which is consistent with groups consisting of a mother and her daughters (subsocial) at some stage and ancestral monogamy, is favored by the haplodiploid genetic sex determination of the Hymenoptera (diploid females and haploid males) and thus may explain why eusociality is common in the Hymenoptera. Ancestral states were also reconstructed for life history characters that have been implicated in the origins of eusociality. A loss of larval diapause during unfavorable seasons or conditions precedes, or coincides with, all but one transition to eusociality. This pattern is confirmed using phylogenetic tests of associations between state transition rates for sweat bees and apid bees. A loss of larval diapause may simply reflect the subsocial route to eusociality since subsociality is defined as females interacting with their adult daughters. A loss of larval diapause and a gain of subsociality may be associated with an extended breeding season that permits the production of at least two broods, which is necessary for helpers to evolve. Adult diapause may also lower the selective barrier to a first-brood daughter becoming a helper. Obligate eusociality meets the definition of a major evolutionary transition, and such transitions have occurred five times in the Hymenoptera.

Case not closed: the mystery of the origin of the carpel

The carpel is a fascinating structure that plays a critical role in flowering plant reproduction and contributed greatly to the evolutionary success and diversification of flowering plants. The remarkable feature of the carpel is that it is a closed structure that envelopes the ovules and after fertilization develops into the fruit which protects, helps disperse, and supports seed development into a new plant. Nearly all plant-based foods are either derived from a flowering plant or are a direct product of the carpel. Given its importance it’s no surprise that plant and evolutionary biologists have been trying to explain the origin of the carpel for a long time. Before carpel evolution seeds were produced on open leaf-like structures that are exposed to the environment. When the carpel evolved in the stem lineage of flowering plants, seeds became protected within its closed structure. The evolutionary transition from that open precursor to the closed carpel remains one of the greatest mysteries of plant evolution. In recent years, we have begun to complete a picture of what the first carpels might have looked like. On the other hand, there are still many gaps in our understanding of what the precursor of the carpel looked like and what changes to its developmental mechanisms allowed for this evolutionary transition. This review aims to present an overview of existing theories of carpel evolution with a particular emphasis on those that account for the structures that preceded the carpel and/or present testable developmental hypotheses. In the second part insights from the development and evolution of diverse plant organs are gathered to build a developmental hypothesis for the evolutionary transition from a hypothesized laminar open structure to the closed structure of the carpel.

Comparative transcriptomics identifies the transcription factors BRANCHED1 and TCP4, as well as the microRNA miR166 as candidate genes involved in the evolutionary transition from dehiscent to indehiscent fruits in Lepidium

Background: Fruits are the seed-bearing structures of flowering plants and are highly diverse in terms of morphology, texture and maturation. Dehiscent fruits split open upon maturation to discharge their seeds while indehiscent fruits are dispersed as a whole. Indehiscent fruits evolved from dehiscent fruits several times independently in the crucifer family (Brassicaceae). The fruits of Lepidium appelianum, for example, are indehiscent while the fruits of the closely related L. campestre are dehiscent. Here, we investigate the molecular and genetic mechanisms underlying the evolutionary transition from dehiscent to indehiscent fruits using these two Lepidium species as model system.Results: We have sequenced the transcriptomes and small RNAs of floral buds, flowers and fruits of L. appelianum and L. campestre and analyzed differentially expressed genes (DEGs) and differently differentially expressed genes (DDEGs). DEGs are genes that show significantly different transcript levels in the same structures (buds, flowers and fruits) in different species, or in different structures in the same species. DDEGs are genes for which the change in expression level between two structures is significantly different in one species than in the other. Comparing the two species, the highest number of DEGs was found in flowers, followed by fruits and floral buds while the highest number of DDEGs was found in fruits versus flowers followed by flowers versus floral buds. Several gene ontology terms related to cell wall synthesis and degradation were overrepresented in different sets of DEGs highlighting the importance of these processes for fruit opening. Furthermore, the fruit valve identity genes FRUITFUL and YABBY3 were among the DEGs identified. Finally, the microRNA miR166 as well as the TCP transcription factors BRANCHED1 (BRC1) and TCP FAMILY TRANSCRIPTION FACTOR 4 (TCP4) were found to be DDEGs.Conclusions: Our study reveals differences in gene expression between dehiscent and indehiscent fruits and uncovers miR166, BRC1 and TCP4 as possible causes for the evolutionary transition from dehiscent to indehiscent fruits in Lepidium.

Comparative transcriptomics identifies the transcription factors BRANCHED1 and TCP4, as well as the microRNA miR166 as candidate genes involved in the evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brassicaceae)

Background: Fruits are the seed-bearing structures of flowering plants and are highly diverse in terms of morphology, texture and maturation. Dehiscent fruits split open upon maturation to discharge their seeds while indehiscent fruits are dispersed as a whole. Indehiscent fruits evolved from dehiscent fruits several times independently in the crucifer family (Brassicaceae). The fruits of Lepidium appelianum, for example, are indehiscent while the fruits of the closely related L. campestre are dehiscent. Here, we investigate the molecular and genetic mechanisms underlying the evolutionary transition from dehiscent to indehiscent fruits using these two Lepidium species as model system. Results: We have sequenced the transcriptomes and small RNAs of floral buds, flowers and fruits of L. appelianum and L. campestre and analyzed differentially expressed genes (DEGs) and differently differentially expressed genes (DDEGs). DEGs are genes that show significantly different transcript levels in the same structures (buds, flowers and fruits) in different species, or in different structures in the same species. DDEGs are genes for which the change in expression level between two structures is significantly different in one species than in the other. Comparing the two species, the highest number of DEGs was found in flowers, followed by fruits and floral buds while the highest number of DDEGs was found in fruits versus flowers followed by flowers versus floral buds. Several gene ontology terms related to cell wall synthesis and degradation were overrepresented in different sets of DEGs highlighting the importance of these processes for fruit opening. Furthermore, the fruit valve identity genes FRUITFUL and YABBY3 were among the DEGs identified. Finally, the microRNA miR166 as well as the TCP transcription factors BRANCHED1 (BRC1) and TCP FAMILY TRANSCRIPTION FACTOR 4 (TCP4) were found to be DDEGs. Conclusions: Our study reveals differences in gene expression between dehiscent and indehiscent fruits and uncovers miR166, BRC1 and TCP4 as possible causes for the evolutionary transition from dehiscent to indehiscent fruits in Lepidium.

A new ant-butterfly symbiosis in the forest canopy fills an evolutionary gap

Myrmecophilous butterflies can establish complex symbiotic relationships with ants. A caterpillar wandering among the brood of the aggressive ponerine ant Neoponera villosa was found inside the core of a nest built in the myrmecophytic bromeliad Aechmea bracteata. This is the first caterpillar found living inside a ponerine ant nest. Its DNA barcode was sequenced, and an integrative approach was used to identify it as Pseudonymphidia agave, a poorly known member of the subtribe Pachythonina in the riodinid tribe Nymphidiini. The cuticle of the tank-like caterpillar lacks projections or tubercles and is covered dorsally by specialized flat setae that form an armor of small plates. Ant-organs potentially related to caterpillar-ant signaling, such as perforated cupola organs and tentacle nectary organs, are present. These morphological traits, together with evidence of social integration (direct contact with host brood, protective morphology, slow movement, no host aggressiveness), suggest that P. agave is a symbiotic, social parasite of N. villosa, preying on its host brood. However, several knowledge gaps remain, including oviposition site, dependence on bromeliad association, steps to colony integration, and larval diet through development. Carnivory has been reported in all known members of the subtribe Pachythonina (caterpillars prey on honeydew-producing hemipterans) suggesting a shift to myrmecophagy inside the ant nests as a possible evolutionary transition.

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

SUMMARYUnderstanding the evolutionary transition to multicellularity is a key problem in evolutionary biology (1,2). While around 25 independent instances of the evolution of multicellular existence are known across the tree of life (3), the ecological conditions that drive such transformations are not well understood. The first known transition to multicellularity occurred approximately 2.5 billion years ago in cyanobacteria (4–6), and today’s cyanobacteria are characterized by an enormous morphological diversity, ranging from single-celled species over simple filamentous to highly differentiated filamentous ones (7,8). While the cyanobacterium Cyanothece sp. ATCC 51142 was isolated from the intertidal zone of the U.S. Gulf Coast as a unicellular species (9), we are first to additionally report a phenotypically mixed strategy where multicellular filaments and unicellular stages alternate. We experimentally demonstrate that the facultative multicellular life cycle depends on environmental conditions, such as salinity and population density, and use a theoretical model to explore the process of filament dissolution. While results predict that the observed response can be caused by an excreted compound in the medium, we cannot fully exclude changes in nutrient availability (as in (10,11)). The best fit modeling results demonstrate a nonlinear effect of the compound, which is characteristic for density-dependent sensing systems (12,13). Further, filament fragmentation is predicted to occur by means of connection cleavage rather than by cell death of every alternate cell. The phenotypic switch between the single-celled and multicellular morphology constitutes an environmentally dependent life cycle, which likely represents an important step en route to permanent multicellularity.