Asymmetry of the male internal reproductive organs in Mantophasmatodea

Background Asymmetries are a widespread phenomenon in otherwise bilaterally symmetric organisms, and investigation of asymmetric structures can help us gather insights into fundamental evolutionary processes such as the selection for morphological novelties caused by behavioural changes. In insects, asymmetric genitalia have evolved in almost every order, and usually it’s the sclerotized parts and most conspicuous male phallic organs that are known to exhibit asymmetries. While external copulatory organs in insects have often been subject to investigations concerning asymmetries and the evolution thereof, internal reproductive structures have received far less attention. Here we describe the internal and external male genitalia in three species of Austrophasmatidae, Mantophasmatodea, using μ-CT imaging and light microscopy. Mantophasmatodea is the most recently discovered insect order, and with 21 species described to date, it is among the smallest insect orders currently known. Results We confirm that male heelwalkers exhibit asymmetries in the external genitalia and associated structures, represented by asymmetric phallic lobes and cerci. Moreover, we found an extreme asymmetry within the internal male genitalia: in all adult males investigated (N = 5), the seminal vesicle, a dilatation of the vas deferens, was only developed on the right side of the male while missing on the left side. Conclusion The false-male-above mating position exhibited by Mantophasmatodea and especially the long copulation duration of ca. 3 days might select for this unusual absence asymmetry of the left seminal vesicle. If this holds true for all heelwalker species, this absence asymmetry constitutes another autapomorphy for Austrophasmatidae or even the insect order Mantophasmatodea.

The Evolution of Hox Genes in Spiralia

The decoding of genomes of a larger number of animal species have provided further insights into the genomic Hox gene organization and with this indicated the evolutionary changes during the radiation of several clades. The expansion of gene expression studies during development and life history stages of more species, complete the picture of the relationship between cluster organisation and temporal and spatial correlation of the Hox activity. Now these results open the opportunity to look deeper into the regulatory pathways that form these patterns and identify what exact changes caused the evolution of the application of this iconical gene set for the evolution of new larval forms and new structures. Here we review recent progress of Hox gene related research in the large clade Spiralia, that comprises Annelida, Mollusca, Lophophorata, Platyhelminthes, Nemertea and others. Albeit their relationship to each other is not resolved yet, there are emerging patterns that indicate that Hox genes are mainly used for patterning late, adult body parts and that Hox genes are often not expressed on the larval stages. Hox genes seem also often recruited for the formation of morphological novelties. Together with the emerging genomic information Hox genes show a much more dynamic evolutionary history than previously assumed.

Ancient gene duplications, rather than polyploidization, facilitate diversification of petal pigmentation patterns in Clarkia gracilis (Onagraceae)

It has been suggested that gene duplication and polyploidization create opportunities for the evolution of novel characters. However, the connections between the effects of polyploidization and morphological novelties have rarely been examined. In this study, we investigated whether petal pigmentation patterning in an allotetraploid Clarkia gracilis has evolved as a result of polyploidization. C. gracilis is thought to be derived through a recent polyploidization event with two diploid species, C. amoena huntiana and an extinct species that is closely related to C. lassenensis. We reconstructed phylogenetic relationships of the R2R3-MYBs (the regulators of petal pigmentation) from two subspecies of C. gracilis and the two purported progenitors, C. a. huntiana and C. lassenensis. The gene tree reveals that these R2R3-MYB genes have arisen through duplications that occurred before the divergence of the two progenitor species, i.e., before polyploidization. After polyploidization and subsequent gene loss, only one of the two orthologous copies inherited from the progenitors was retained in the polyploid, turning it to diploid inheritance. We examined evolutionary changes in these R2R3-MYBs and in their expression, which reveals that the changes affecting patterning (including expression domain contraction, loss-of-function mutation, cis-regulatory mutation) occurred after polyploidization within the C. gracilis lineages. Our results thus suggest that polyploidization itself is not necessary in producing novel petal color patterns. By contrast, duplications of R2R3-MYB genes in the common ancestor of the two progenitors have apparently facilitated diversification of petal pigmentation patterns.

Developmental Capacity and the Early Evolution of Animals

Disentangling the factors underlying the appearance of macroscopic, often skeletonized, bilaterians during the Ediacaran-Cambrian diversification of animals requires carefully parsing the contributions of ecological opportunity, environmental potential and developmental capacity. The early evolution of animals involved the introduction of genomic, developmental, morphologic and behavioral novelties, identified as the individuation of new characters, which led to the construction of new ecological networks (innovation). Here I employ a recently introduced conceptual framework for novelty and individuation that distinguishes between potentiation, novelty, innovation and adaptive adjustments to the Ediacaran-Cambrian radiation, and focus on the roles of potentiation and novelty in the expansion of developmental capacity. Comparative developmental studies combined with molecular clock estimates and data from the fossil record suggest that developmental capacity, the potential to generate a range of morphologies, may expand rapidly through developmental novelties without leading directly to morphological novelties, or to innovation. The expected patterns from this framework are markedly different from those in adaptive radiation scenarios.Thematic collection: This article is part of the Advances in the Cambrian Explosion collection available at: https://www.lyellcollection.org/cc/advances-cambrian-explosion

Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks

Hox genes are key developmental regulators that are involved in establishing morphological features during animal ontogeny. They are commonly expressed along the anterior–posterior axis in a staggered, or collinear, fashion. In mollusks, the repertoire of body plans is widely diverse and current data suggest their involvement during development of landmark morphological traits in Conchifera, one of the two major lineages that comprises those taxa that originated from a uni-shelled ancestor (Monoplacophora, Gastropoda, Cephalopoda, Scaphopoda, Bivalvia). For most clades, and bivalves in particular, data on Hox gene expression throughout ontogeny are scarce. We thus investigated Hox expression during development of the quagga mussel, Dreissena rostriformis, to elucidate to which degree they might contribute to specific phenotypic traits as in other conchiferans. The Hox/ParaHox complement of Mollusca typically comprises 14 genes, 13 of which are present in bivalve genomes including Dreissena. We describe here expression of 9 Hox genes and the ParaHox gene Xlox during Dreissena development. Hox expression in Dreissena is first detected in the gastrula stage with widely overlapping expression domains of most genes. In the trochophore stage, Hox gene expression shifts towards more compact, largely mesodermal domains. Only few of these domains can be assigned to specific developing morphological structures such as Hox1 in the shell field and Xlox in the hindgut. We did not find traces of spatial or temporal staggered expression of Hox genes in Dreissena. Our data support the notion that Hox gene expression has been coopted independently, and to varying degrees, into lineage-specific structures in the respective conchiferan clades. The non-collinear mode of Hox expression in Dreissena might be a result of the low degree of body plan regionalization along the bivalve anterior–posterior axis as exemplified by the lack of key morphological traits such as a distinct head, cephalic tentacles, radula apparatus, and a simplified central nervous system.

Developmental hourglass and heterochronic shifts in fin and limb development

How genetic changes are linked to morphological novelties and developmental constraints remains elusive. Here we investigate genetic apparatuses that distinguish fish fins from tetrapod limbs by analyzing transcriptomes and open chromatin regions (OCRs). Specifically, we compared mouse forelimb buds with the pectoral fin buds of an elasmobranch, the brown-banded bamboo shark (Chiloscyllium punctatum). A transcriptomic comparison with an accurate orthology map revealed both a mass heterochrony and hourglass-shaped conservation of gene expression between fins and limbs. Furthermore, open-chromatin analysis suggested that access to conserved regulatory sequences is transiently increased during mid-stage limb development. During this stage, stage-specific and tissue-specific OCRs were also enriched. Together, early and late stages of fin/limb development are more permissive to mutations than middle stages, which may have contributed to major morphological changes during the fin-to-limb evolution. We hypothesize that the middle stages are constrained by regulatory complexity that results from dynamic and tissue-specific transcriptional controls.

Lamprey Lecticans Link New Vertebrate Genes to the Origin and Elaboration of Vertebrate Tissues

ABSTRACTThe evolution of vertebrates from an invertebrate chordate ancestor involved the evolution of new organs, tissues, and cell types. It was also marked by the origin and duplication of new gene families. If, and how, these morphological and genetic innovations are related is an unresolved question in vertebrate evolution. Hyaluronan is an extracellular matrix (ECM) polysaccharide important for water homeostasis and tissue structure. Vertebrates possess a novel family of hyaluronan binding proteins called Lecticans, and studies in jawed vertebrates (gnathostomes) have shown they function in many of the cells and tissues that are unique to vertebrates. This raises the possibility that the origin and/or expansion of this gene family helped drive the evolution of these vertebrate novelties. In order to better understand the evolution of the lectican gene family, and its role in the evolution of vertebrate morphological novelties, we investigated the phylogeny, genomic arrangement, and expression patterns of all lecticans in the sea lamprey (Petromyzon marinus), a jawless vertebrate. Though both P. marinus and gnathostomes have four lecticans, our phylogenetic and syntenic analyses suggest lamprey lecticans are the result of one or more cyclostome-specific duplications. Despite the independent expansion of the lamprey and gnathostome lectican families, we find highly conserved expression of lecticans in vertebrate-specific and mesenchyme-derived tissues. We also find that, unlike gnathostomes, lamprey expresses its lectican paralogs in distinct subpopulations of head skeleton precursors, potentially reflecting an ancestral diversity of skeletal tissue types. Together, these observations suggest that the ancestral pre-duplication lectican had a complex expression pattern, functioned to support mesenchymal histology, and likely played a role in the evolution of vertebrate-specific cell and tissue types.

Pattern of sucker development in cuttlefishes

Background : Morphological novelties have been acquired through evolutionary processes and related to the adaptation of new life-history strategies with new functions of the bodyparts. Cephalopod molluscs such as octopuses, squids and cuttlefishes possess unique morphological characteristics. Among those novel morphologies, in particular, suckers arranged along the oral side of each arm possess multiple functions, such as capturing prey and locomotion, so that the sucker morphology is diversified among species, depending on their ecological niche. However, the detailed developmental process of sucker formation has remained unclear, although it is known that new suckers are formed or added during both embryonic and postembryonic development. In the present study, therefore, focusing on two cuttlefish species, Sepia esculenta and S. lycidas , in which the sucker morphology is relatively simple, morphological and histological observations were carried out during embryonic and postembryonic development to elucidate the developmental process of sucker formation and to compare them among other cephalopod species. Results : The observations in both species clearly showed that the newly formed suckers were added on the oral side of the most distal tip of each arm during embryonic and postembryonic development. On the oral side of the arm tip, the epithelial tissue became swollen to form a ridge along the proximal-distal axis (sucker field ridge). Next to the sucker field ridge, there were small dome-shaped bulges that are presumed to be the sucker buds. Toward the proximal direction, the buds became functional suckers, in which the inner tissues differentiated to form the complex sucker structures. During postembryonic development, on both sides of the sucker field ridge, epithelial tissues extended to form a sheath, covering the ridge for protection of undifferentiated suckers. Conclusions : The developmental process of sucker formation, in which sucker buds are generated from a ridge structure (sucker field ridge) on the oral side at the distal-most arm tip, was shared in both cuttlefish species, although some minor heterochronic shifts of the developmental events were detected between the two species.