Origin Of Novel Structures Research Articles

The Daphnia carapace and other novel structures evolved via the cryptic persistence of serial homologs

Understanding how novel structures arise is a central question in evolution. Novel structures are often defined as structures that are not derived from (homologous to) any structure in the ancestor.1 The carapace of the crustacean Daphnia magna is a bivalved "cape" of exoskeleton. Shiga etal.2 proposed that the carapace of crustaceans like Daphnia and many other plate-like outgrowths in arthropods are novel structures that arose through the repeated co-option of genes like vestigial that also pattern insect wings.2-4 To determine whether the Daphnia carapace is a novel structure, we compare previous functional work2 with the expression of genes known to pattern the proximal leg region (pannier, araucan, and vestigial)5,6 between Daphnia, Parhyale, and Tribolium. Our results suggest that the Daphnia carapace did not arise by co-option but instead derived from an exite (lateral leg lobe) that emerges from an ancestral proximal leg segment that was incorporated into the Daphnia body wall. The Daphnia carapace, therefore, appears to be homologous to the Parhyale tergal plate and the insect wing.5 Remarkably, the vestigial-positive tissue that gives rise to the Daphnia carapace appears to be present in Parhyale7 and Tribolium as a small, inconspicuous protrusion. Thus, rather than a novel structure resulting from gene co-option, the Daphnia carapace appears to have arisen from a shared, ancestral tissue (morphogenetic field) that persists in a cryptic state in other arthropod lineages. Cryptic persistence of unrecognized serial homologs may thus be a general solution for the origin of novel structures.

Stress-Induced Evolutionary Innovation: A Mechanism for the Origin of Cell Types.

Understanding the evolutionary role of environmentally induced phenotypic variation (i.e., plasticity) is an important issue in developmental evolution. A major physiological response to environmental change is cellular stress, which is counteracted by generic stress reactions detoxifying the cell. A model, stress-induced evolutionary innovation (SIEI), whereby ancestral stress reactions and their corresponding pathways can be transformed into novel structural components of body plans, such as new cell types, is described. Previous findings suggest that the cell differentiation cascade of a cell type critical to pregnancy in humans, the decidual stromal cell, evolved from a cellular stress reaction. It is hypothesized that the stress reaction in these cells was elicited ancestrally via inflammation caused by embryo attachment. The present study proposes that SIEI is a distinct form of plasticity-based evolutionary change leading to the origin of novel structures rather than adaptive transformation of pre-existing characters.

Exceptional preservation and the fossil record of tetrapod integument.

The fossil record of exceptionally preserved soft tissues in Konservat-Lagerstätten provides rare yet significant insight into past behaviours and ecologies. Such deposits are known to occur in bursts rather than evenly through time, but reasons for this pattern and implications for the origins of novel structures remain unclear. Previous assessments of these records focused on marine environments preserving chemically heterogeneous tissues from across animals. Here, we investigate the preservation of skin and keratinous integumentary structures in land-dwelling vertebrates (tetrapods) through time, and in distinct terrestrial and marine depositional environments. We also evaluate previously proposed biotic and abiotic controls on the distribution of 143 tetrapod Konservat-Lagerstätten from the Permian to the Pleistocene in a multivariate framework. Gap analyses taking into account sampling intensity and distribution indicate that feathers probably evolved close to their first appearance in the fossil record. By contrast, hair and archosaur filaments are weakly sampled (five times less common than feathers), and their origins may significantly pre-date earliest known occurrences in the fossil record. This work suggests that among-integument variation in preservation can bias the reconstructed first origins of integumentary novelties and has implications for predicting where, and in what depositional environments, to expect further discoveries of exquisitely preserved tetrapod integument.

Furcation, field-splitting, and the evolutionary origins of novelty in arthropod photoreceptors

Arthropod photoreceptor evolution is a prime example of how evolution has used existing components in the origin of new structures. Here, we outline a comparative approach to understanding the mutational origins of novel structures, describing multiple examples from arthropod photoreceptor evolution. We suggest that developmental mechanisms have often split photoreceptors during evolution (field-splitting) and we introduce “co-duplication” as a null model for the mutational origins of photoreceptor components. Under co-duplication, gene duplication events coincide with the origin of a higher level structure like an eye. If co-duplication is rejected for a component, that component probably came to be used in a new photoreceptor through regulatory mutations. If not rejected, a gene duplication mutation may have allowed the component to be used in a new structure. In multiple case studies in arthropod photoreceptor evolution, we consistently reject the null hypothesis of co-duplication of genetic components and photoreceptors. Nevertheless, gene duplication events have in some cases occurred later, allowing divergence of photoreceptors. These studies provide a new perspective on the evolution of arthropod photoreceptors and provide a comparative approach that generalizes to the study of any evolutionary novelty.

Evaluating paedomorphic heterochrony in trilobites: the case of the diminutive trilobite Flexicalymene retrorsa minuens from the Cincinnatian Series (Upper Ordovician), Cincinnati region

Flexicalymene retrorsa minuens from the uppermost 3 m of the Waynesville Formation of the Cincinnatian Series (Upper Ordovician) of North America lived approximately 445 Ma and exhibited marked reduction in maximum size relative to its stratigraphically subjacent sister subspecies, Flexicalymene retrorsa retrorsa. Phylogenetic analysis is consistent with the notion that F. retrorsa retrorsa was the ancestor of F. retrorsa minuens. F. retrorsa minuens has been claimed to differ from F. retrorsa retrorsa"in size alone," and thus presents a plausible example of global paedomorphic evolution in trilobites. Despite strong similarity in the overall form of the two subspecies, F. retrorsa minuens is neither a dwarf nor a simple progenetic descendant of F. retrorsa retrorsa. More complex patterns of global heterochronic paedomorphosis, such as a neotonic decrease in the rate of progress along a common ontogenetic trajectory with respect to size, coupled with growth cessation at a small size, "sequential" progenesis, or non-uniform changes in the rate of progress along a shared ontogenetic trajectory with respect to size, can also be rejected. Rather, differences between these subspecies are more consistent with localized changes in rates of character development than with a global heterochronic modification of the ancestral ontogeny. The evolution of F. retrorsa minuens from F. retrorsa retrorsa was largely dominated by modifications of the development of characters already evident in the ancestral ontogeny, not by the origin of novel structures. Factors promoting size reduction in F. retrorsa minuens appear to have been specific to this subspecies, because other co-occurring taxa, including other trilobite species, do not show marked differences in mean size.

A PHYLOGENETIC HOT SPOT FOR EVOLUTIONARY NOVELTY IN MIDDLE AMERICAN TREEFROGS

Among the various types of evolutionary changes in morphology, the origin of novel structures may be the most rare and intriguing. Here we show statistically that the origins of different novel structures may be correlated and phylogenetically clustered into "hot spots" of evolutionary novelty, in a case study involving skull elements in treefrogs. We reconstruct phylogenetic relationships within a clade of Middle American treefrogs based on data from 10 nuclear and four mitochondrial genes and then analyze morphological evolution across this tree. New cranial elements are rare among anurans and tetrapods in general, but three novel elements have evolved within this clade, with a 40% increase in the number of skull roof elements in some species. Two of these elements also evolved in a related clade of treefrogs, and these two novel elements may have each evolved repeatedly within one or both clades. The molecular phylogeny suggests striking homoplasy in cranial morphology and shows that parsimony and Bayesian analyses of the morphological data have produced misleading results with strong statistical support. The origins of the novel elements are associated with an overall increase in the ossification of dermal skull roof elements (suggesting peramorphosis) and with the evolution of a novel adaptive behavior. Our study may be the first to statistically document significant phylogenetic clustering and correlation in the origins of novel structures, and to demonstrate the strongly misleading effects of peramorphosis on phylogenetic analysis.

Evolution and development: some insights from evolutionary theory

Developmental biology and evolutionary biology are both mature integrative disciplines which started in the 19th century and then followed parallel and independent scientific pathways. Recently, a genetical component has stepped into both disciplines (developmental genetics and evolutionary genetics) pointing out the need for future convergent maturation. Indeed, the Evo-Devo approach is becoming popular among developmental biologists, based on the facts that distant groups share a common ancestry, that precise phylogenies can be worked out and that homologous genes often play similar roles during the development of very different organisms. In this essay, I try to show that the real future of Evo-Devo thinking is still broader. The evolutionary theory is a set of diverse concepts which can and should be used in any biological field. Evolutionary thinking trains to ask << why >> questions and to provide logical and plausible answers. It can shed some light on a diversity of general problems such as how to distinguish homologies from analogies, the costs and benefits of multicellularity, the origin of novel structures (e.g. the head), or the evolution of sexual reproduction. In the next decade, we may expect a progressive convergence between developmental genetics and quantitative genetics.