Serially Homologous Research Articles

Testing Empirical Support for Evolutionary Models that Root the Tree of Life

Trees of life (ToLs) can only be rooted with direct methods that seek optimization of character state information in ingroup taxa. This involves optimizing phylogenetic tree, model and data in an exercise of reciprocal illumination. Rooted ToLs have been built from a census of protein structural domains in proteomes using two kinds of models. Fully-reversible models use standard-ordered (additive) characters and Wagner parsimony to generate unrooted trees of proteomes that are then rooted with Weston’s generality criterion. Non-reversible models directly build rooted trees with unordered characters and asymmetric stepmatrices of transformation costs that penalize gain over loss of domains. Here, we test the empirical support for the evolutionary models with character state reconstruction methods using two published proteomic datasets. We show that the reversible models match reconstructed frequencies of character change and are faithful to the distribution of serial homologies in trees. In contrast, the non-reversible models go counter to trends in the data they must explain, attracting organisms with large proteomes to the base of the rooted trees while violating the triangle inequality of distances. This can lead to serious reconstruction inconsistencies that show model inadequacy. Our study highlights the aprioristic perils of disposing of countering evidence in natural history reconstruction.

Serial Homology and Correlated Characters in Morphological Phylogenetics: Modeling the Evolution of Dental Crests in Placentals.

Accurate modeling of the complexity of morphological evolution is crucial for morphological phylogenetics and for performing tests on a wide variety of evolutionary scenarios. In this context, morphological integration and the problem of correlated categorical characters represent a major challenge. In particular, the magnitude and implications of correlations among serially homologous structures such as teeth have been much debated but were never tested statistically within a broad phylogenetic context. Here, we present a large-scale empirical study analyzing the serial variation of cingular crests on successive molars (M1, M2, and M3) of 274 placental species in a phylogenetic context. Both likelihood analyses and analysis of phylogenetic co-distributions demonstrated highly correlated evolution in the entire sample and thus the non-independence of these serial features at a macroevolutionary scale. Likelihood analyses show that their serial variation should be better scored within a single composite character model with constrained paths for transitions enabling simultaneous changes on all three molars, which suggests a strong developmental or genetic integration. These results are congruent with current genetic and developmental knowledge related to dental morphological variation and call into question the frequent use of separate characters scored on serially homologous structures of the dentition in phylogenetic analyses. Overall, they provide long-overdue and clear empirical evidence that in-depth studies of patterns of integration constitute an essential step toward more realistic character construction and modeling. This approach is critical for more accurate morphological phylogenetics and, more generally, for testing macroevolutionary scenarios on groups of correlated characters.

Reigitherium (Meridiolestida, Mesungulatoidea) an Enigmatic Late Cretaceous Mammal from Patagonia, Argentina: Morphology, Affinities, and Dental Evolution

New dental and dentary fossils collected in the Upper Cretaceous La Colonia Formation in central Patagonia provide new evidence on the morphology, feeding ecology, and relationships of the enigmatic mammal Reigitherium. The newly discovered specimens described here include elements of the upper dentition and several partial dentaries, elucidating fundamental questions of serial homology and postcanine dental formula (four premolars and three molars). This new evidence supports a nested position of Reigitherium within the advanced meridiolestidan clade Mesungulatoidea. Apomorphic features of the upper and lower molariform elements include intense enamel crenulation circumscribed within the primary trigon and trigonid, elevated cingulids, and the neomorphic appearance of cusps/cuspulids, all of which increase overall crown complexity. A Dental Topography Analysis comparing Reigitherium and its sister taxon Peligrotherium to Cretaceous and Cenozoic therians demonstrates functional similarity between the mesungulatoids and South American marsupial taxa that succeed them in the small-to medium-sized herbivore niche during the Paleocene. Previous taxonomic attributions of Reigitherium are discussed and comparisons with other meridiolestidans highlight the remarkable radiation of this group in the Cretaceous of South America.

Comments on the Serial Homology and Homologues of Vertebral Lateral Projections in Crocodylia (Eusuchia).

The literature on crocodylian anatomy presents the transverse process in an ambiguous meaning, which could represent all lateral expansions derived from the neural arch, including vertebrae from cervical to caudal series, or in a more restrictive meaning, being applied only to lumbar vertebrae. The lateral expansion of sacral and caudal vertebrae usually referred to as the transverse process has been discovered to be fused ribs, bringing more ambiguity to this term. Therefore, with the lack of a definition for transverse process and other associated terms, the present work aims to propose a nomenclatural standardization, as well as definitions and biological meaning, for vertebral rib related structures. Vertebra obtained from museum collections from a total of 87 specimens of 22 species of all extant Crocodylia genera were studied. All vertebrae, except cervical and first three dorsal, exhibit transverse processes. The transverse process is more developed in dorsal and lumbar vertebrae than in sacral and caudal vertebrae in which it is suppressed by the fused ribs. The serial homology hypotheses here proposed can also be aplied to other Crurotarsi and saurischian dinosaurs specimens. This standardization clarifies the understand of the serial homology among those homotypes, and reduces the ambiguity and misleadings in future work comparisons. Anat Rec, 301:1203-1215, 2018. © 2018 Wiley Periodicals, Inc.

The fine structure of ‘homology’

There is long-standing conflict between genealogical and developmental accounts of homology. This paper provides a general framework that shows that these accounts are compatible and clarifies precisely how they are related. According to this framework, understanding homology requires both (a) an abstract genealogical account that unifies the application of the term to all types of characters used in phylogenetic systematics and (b) locally enriched accounts that apply only to specific types of characters. The genealogical account serves this unifying role by relying on abstract notions of ‘descent’ and ‘character’. As a result, it takes for granted the existence of such characters. This requires theoretical justification that is provided by enriched accounts, which incorporate the details by which characters are inherited. These enriched accounts apply to limited domains (e.g. genes and proteins, or body parts), providing the needed theoretical justification for recognizing characters within that domain. Though connected to the genealogical account of homology in this way, enriched accounts include phenomena (e.g. serial homology, paralogy, and xenology) that fall outside the scope of the genealogical account. They therefore overlap, but are not nested within, the genealogical account. Developmental accounts of homology are to be understood as enriched accounts of body part homology. Once they are seen in this light, the conflict with the genealogical account vanishes. It is only by understanding the fine conceptual structure undergirding the many uses of the term ‘homology’ that we can understand how these uses hang together.

Plywood‐like shell microstructures in hyoliths from the middle Cambrian (Drumian) Gowers Formation, Georgina Basin, Australia

AbstractHyoliths are a group of Palaeozoic fossils with calcareous shells whose affinities remain controversial. As their shells were originally aragonitic, their fossils are usually coarsely recrystallized, and few data on their microstructure are available. We report hyoliths from the middle Cambrian (Drumian, Floran) Gowers Formation of the eastern Georgina Basin, Queensland. These are preserved as phosphatic internal moulds, often with the inner layers of the shell also partly replaced by phosphate. Microstructural details preserved by this early diagenetic phosphatization show that these hyolith conchs were originally composed of fibrous crystallites, c. 0.5 μm wide, parallel to one another and to the inner surface of the shell. In several species, the fibres are arranged in a plywood‐like structure composed of multiple lamellae with a different fibre orientation in each lamella: often they are transversely oriented (relative to the long axis of the conch) in the inner part of the wall and longitudinally oriented in the outer part. Opercula also show a microstructure of parallel fibres. The lamello‐fibrillar microstructure we report from hyoliths is reminiscent of microstructures of many Cambrian molluscs; that this microstructure is found in both conchs and opercula suggests that these structures are serial homologues of one another, and in this respect they resemble brachiopod valves. As with many other biological plywoods, the hyolith shell probably records self‐organization in a liquid‐crystal‐like organic matrix. This provided a straightforward way to construct a material that could resist stresses from different directions, offering an effective defence against predators.

Progressive derivation of serially homologous neuroblast lineages in the gnathal CNS of Drosophila.

Along the anterior-posterior axis the central nervous system is subdivided into segmental units (neuromeres) the composition of which is adapted to their region-specific functional requirements. In Drosophila melanogaster each neuromere is formed by a specific set of identified neural stem cells (neuroblasts, NBs). In the thoracic and anterior abdominal region of the embryonic ventral nerve cord segmental sets of NBs resemble the ground state (2nd thoracic segment, which does not require input of homeotic genes), and serial (segmental) homologs generate similar types of lineages. The three gnathal head segments form a transitional zone between the brain and the ventral nerve cord. It has been shown recently that although all NBs of this zone are serial homologs of NBs in more posterior segments, they progressively differ from the ground state in anterior direction (labial > maxillary > mandibular segment) with regard to numbers and expression profiles. To study the consequences of their derived characters we traced the embryonic lineages of gnathal NBs using the Flybow and DiI-labelling techniques. For a number of clonal types serial homology is rather clearly reflected by their morphology (location and projection patterns) and cell specific markers, despite of reproducible segment-specific differences. However, many lineages, particularly in the mandibular segment, show a degree of derivation that impedes their assignment to ground state serial homologs. These findings demonstrate that differences in gene expression profiles of gnathal NBs go along with anteriorly directed progressive derivation in the composition of their lineages. Furthermore, lineage sizes decrease from labial to mandibular segments, which in concert with decreasing NB-numbers lead to reduced volumes of gnathal neuromeres, most significantly in the mandibular segment.

Dual evolutionary origin of insect wings supported by an investigation of the abdominal wing serial homologs in Tribolium

The origin of insect wings is still a highly debated mystery in biology, despite the importance of this evolutionary innovation. There are currently two prominent, but contrasting wing origin hypotheses (the tergal origin hypothesis and the pleural origin hypothesis). Through studies in the Tribolium beetle, we have previously obtained functional evidence supporting a third hypothesis, the dual origin hypothesis. Although this hypothesis can potentially unify the two competing hypotheses, it requires further testing from various fields. Here, we investigated the genetic regulation of the tissues serially homologous to wings in the abdomen, outside of the appendage-bearing segments, in Tribolium We found that the formation of ectopic wings in the abdomen upon homeotic transformation relies not only on the previously identified abdominal wing serial homolog (gin-trap), but also on a secondary tissue in the pleural location. Using an enhancer trap line of nubbin (a wing lineage marker), we were able to visualize both of these two tissues (of tergal and pleural nature) contributing to form a complete wing. These results support the idea that the presence of two distinct sets of wing serial homologs per segment represents an ancestral state of the wing serial homologs, and can therefore further support a dual evolutionary origin of insect wings. Our analyses also uncovered detailed Hox regulation of abdominal wing serial homologs, which can be used as a foundation to elucidate the molecular mechanisms that have facilitated the evolution of bona fide insect wings, as well as the diversification of other wing serial homologs.

Similarity of morphological composition and developmental patterning in paired fins of the elephant shark

Jawed vertebrates, or gnathostomes, have two sets of paired appendages, pectoral and pelvic fins in fishes and fore- and hindlimbs in tetrapods. As for paired limbs, paired fins are purported serial homologues, and the advent of pelvic fins has been hypothesized to have resulted from a duplication of the developmental mechanisms present in the pectoral fins, but re-iterated at a posterior location. Developmental similarity of gene expression between pectoral and pelvic fins has been documented in chondrichthyans, but a detailed morphological description of the progression of paired fin development for this group is still lacking. We studied paired fin development in an ontogenetic series of a phylogenetically basal chondrichthyan, the elephant shark Callorhinchus milii. A strong similarity in the morphology and progression of chondrification between the pectoral and pelvic fins was found, which could be interpretated as further evidence of serial homology in paired fins, that could have arisen by duplication. Furthermore, this high degree of morphological and developmental similarity suggests the presence of morphological and developmental modules within paired fins, as observed in paired limbs. This is the first time morphological and developmental modules are described for the paired fins of chimaeras.

Evolutionary shifts in gene expression decoupled from gene duplication across functionally distinct spider silk glands

Spider silk synthesis is an emerging model for the evolution of tissue-specific gene expression and the role of gene duplication in functional novelty, but its potential has not been fully realized. Accordingly, we quantified transcript (mRNA) abundance in seven silk gland types and three non-silk gland tissues for three cobweb-weaving spider species. Evolutionary analyses based on expression levels of thousands of homologous transcripts and phylogenetic reconstruction of 605 gene families demonstrated conservation of expression for each gland type among species. Despite serial homology of all silk glands, the expression profiles of the glue-forming aggregate glands were divergent from fiber-forming glands. Also surprising was our finding that shifts in gene expression among silk gland types were not necessarily coupled with gene duplication, even though silk-specific genes belong to multi-paralog gene families. Our results challenge widely accepted models of tissue specialization and significantly advance efforts to replicate silk-based high-performance biomaterials.

Serial and special: Comparison of podomeres and muscles in tactile vs walking legs of whip scorpions (Arachnida, Uropygi)

Uropygi are one of a small number of taxa within the Arachnida that do not walk on four pairs of post-pedipalpal legs. The second, third and fourth pair are used for locomotion, while the first pair has evolved into a pair of elongated and antenniform sensory appendages extensively covered with sensilla. The podomeres of this first pair of legs display about six additional tarsomeres, and the terminal claw-like apotele is reduced. A patella as found in the posterior three pairs of legs, and in all four pairs of legs of the closely related Amblypygi and Araneae, appears to be absent. This has caused some authors to assume that the patella has fused with the tibia to form a so-called “patellotibia”. However, this hypothesis is controversial, and various authors have used a labelling of the podomeres of the antenniform pair of legs including a “patella”. To shed more light on the matter, we analyse here the morphology of the four pairs of post-pedipalpal legs in Mastigoproctus giganteus. Our study uses micro-computed tomography (μCT)-based 3D reconstructions of the intrinsic muscles and cuticle components of the podomeres to describe and compare these morphological structures. The evolutionary changes undergone by the podomeres and the muscular system in the antenniform legs of Thelyphonidae are discussed and the homologous identity between podomeres is discussed on the basis of the hypothesis of serial homology. Our findings imply a refutal of the patellotibia hypothesis.

The insect antenna: segmentation, patterning and positional homology

The basic mechanism by which the antennal flagellum is subdivided into flagellomeres is probably the same in all insects, irrespective of whether the process occurs in the embryo, in the eye/antenna imaginal disc, or through a series of post-embryonic increments punctuated by moults. The ultimate origin of (all?) flagellomeres is the first antennomere following the pedicel, from which split off in apical direction new primary flagellomeres, each of which is eventually the source of secondary flagellomeres, according to specific spatial and temporal patterns subject to heterochrony. Only a detailed knowledge of the underlying segmentation processes could provide the ultimate background for determining positional homology between flagellomeres of two antennae with different number of antennomeres. The antennae of the Heteroptera are likely re-segmented, as their second antennomere seems to include a flagellar component. The larval antennae of the holometabolans are temporal serial homologues of those of the adult, but their segmental composition is problematic. Significant progress will be done by understanding what differentiates antennomeres that divide, either embryonically or post-embryonically, from those that do not; and by discovering whether the spatial and temporal pattern of division along the flagellum depends on local cues, or on signals travelling along the whole proximo-distal axis of the appendage.

What serial homologs can tell us about the origin of insect wings.

Although the insect wing is a textbook example of morphological novelty, the origin of insect wings remains a mystery and is regarded as a chief conundrum in biology. Centuries of debates have culminated into two prominent hypotheses: the tergal origin hypothesis and the pleural origin hypothesis. However, between these two hypotheses, there is little consensus in regard to the origin tissue of the wing as well as the evolutionary route from the origin tissue to the functional flight device. Recent evolutionary developmental (evo-devo) studies have shed new light on the origin of insect wings. A key concept in these studies is “serial homology”. In this review, we discuss how the wing serial homologs identified in recent evo-devo studies have provided a new angle through which this century-old conundrum can be explored. We also review what we have learned so far from wing serial homologs and discuss what we can do to go beyond simply identifying wing serial homologs and delve further into the developmental and genetic mechanisms that have facilitated the evolution of insect wings.

Genetic and environmental integration of the hawkmoth pollination syndrome in Ruellia humilis (Acanthaceae).

The serial homology of floral structures has made it difficult to assess the relative contributions of selection and constraint to floral integration. The interpretation of floral integration may also be clouded by the tacit, but largely untested, assumption that genetic and environmental perturbations affect trait correlations in similar ways. In this study, estimates of both the genetic and environmental correlations between components of the hawkmoth pollination syndrome are presented for chasmogamous flowers of Ruellia humilis , including two levels of control for serial homology. A greenhouse population for quantitative genetic analysis was generated by a partial diallel cross between field-collected plants. An average of 634 chasmogamous flowers were measured for each of eight floral traits that contribute to the hawkmoth syndrome. Genetic correlations (across parents) and environmental correlations (across replicate flowers) were estimated by restricted maximum likelihood. Stigma height, anther height and floral tube length were very tightly integrated in their responses to both genetic and environmental perturbations. The inclusion of floral disc width as a control for serial homology suggests this integration is an adaptive response to correlational selection imposed by pollinators. In contrast, integration of non-homologous traits was low. Furthermore, when comparisons between the dimensions of serially homologous structures were excluded, the genetic and environmental correlation matrices showed little congruence. The results suggest that hawkmoths have imposed strong correlational selection on floral traits involved in the deposition and removal of pollen, and that this is a consequence of stabilizing selection on the relative positions of stigmas and anthers in the face of substantial flower size variation. Low integration of other floral traits, and conflicting patterns of genetic and environmental correlations among these traits, suggest weak or no correlational selection within the range of variability expressed within a population.

Out on a limb: bandicoot limb co-variation suggests complex impacts of development and adaptation on marsupial forelimb evolution.

Marsupials display far less forelimb diversity than placentals, possibly because of the laborious forelimb-powered climb to the pouch performed by most marsupial neonates. This is thought to result in stronger morphological integration (i.e., higher co-variance) within the marsupial forelimb skeleton, and lower integration between marsupial fore- and hind limbs, compared to other mammals. Possible mechanisms for this constraint are a fundamental developmental change in marsupial limb patterning, or alternatively more immediate perinatal biomechanical and metabolic requirements. In the latter case, peramelid marsupials (bandicoots), which have neonates that climb very little, should show lower within-limb and higher between-limb integration, compared to other marsupials. We tested this in four peramelid species and the related bilby, using partial correlation analyses of between-landmark linear measurements of limb bones, and Procrustes-based two-block partial least-squares analysis (2B-PLS) of limb bone shapes using the same landmarks. We find extensive between-limb integration in partial correlation analyses of only bone lengths, consistent with a reduction of a short-term biomechanical/allocation constraint in peramelid forelimbs. However, partial correlations of bone proportions and 2B-PLS reveal extensive shape divergence between correlated bone pairs. This result contradicts expectations of developmental constraints or serial homology, instead suggesting a function-driven integration pattern. Comparing visualizations from cross-species principal components analysis and 2B-PLS, we tentatively identify selection for digging and half-bounding as the main driver of bandicoot limb integration patterning. This calls for further assessments of functional versus developmental limb integration in marsupials with a more strenuous neonatal climb to the pouch.

Mature larva of Stenichnus godarti (Latreille) (Coleoptera: Staphylinidae,Scydmaeninae): redescription, hypothesis of displaced epicranial suture and alternative interpretation of homology between chaetotaxic structures.

The mature larva of Stenichnus godarti is redescribed on the basis of a shed larval skin; identification was made by rearing the adult. New data on the life history of St. godarti are provided, including feeding behavior of the larva and adult and longevity of the adult under laboratory conditions. Possible serial homology of chaetotaxic structures across body segments is discussed, and morphological structures of immature St. godarti are compared with those of previously described St. collaris. It is concluded that despite structural similarities and some chaetotaxic structures (mainly on the antennae, mouthparts, legs and thoracic sternites) shared by St. godarti and St. collaris, differences in some important body regions are so profound that it is difficult to draw homologies between setal pattern on the head, thoracic and most of the abdominal tergites, based solely on topological evidence. Differences in the chaetotaxy of the head are especially puzzling and a hypothesis of displaced frontal arms of the epicranial suture is proposed, assuming homology between the presutural setae of St. godarti with postsutural setae of St. collaris. Furthermore, alternative interpretations of dorsal thoracic setae are discussed.

Playing with Black and Yellow: The Evolvability of a Batesian Mimicry

Irrespective of the selective advantage deriving from similar color pattern, the evolution of Batesian (and Mullerian) mimicry between distantly related insects groups has been perhaps facilitated by the availability to both models and mimics of similar pattern units more likely to be expressed, and to be modified in parallel ways, due to shared developmental constraints. We explore this hypothesis in a comparison of units of black-and-yellow color patterns between wasps (Vespidae) and those syrphids (Syrphidae) that are considered to be their Batesian mimics. As a proxy for evolvability we analyzed the co-occurrence of multiple color pattern within species (either as serial homologues or as expression of intraspecific variation) in 203 species of syrphids and 127 species of wasps. In both the wasps and the syrphids, the most frequent black-and-yellow patterns on the abdomen—all shared between the two insect groups—are also the most extensively linked in the networks of intraspecific co-occurrence, but are not the same in the two insect groups: in accordance with our hypothesis, this suggests positively biased evolvability.

Description of the second- and third-instar larva of South African Stenomastigus longicornis (Boheman) (Coleoptera: Staphylinidae, Scydmaeninae).

The second- and third-instar larvae of the South African species of Mastigini, Stenomastigus longicornis, are described. The serial homology of chaetotaxic structures and differences between larval instars are discussed. The larva of Stenomastigus is very similar to that of Palaeostigus, but differences in proportions of body parts, number of setae on the head, thorax and abdomen and possibly also the shape of the antennal sensory appendage can be used to distinguish them. A frontal impression surrounded by modified setae with greatly enlarged surface, presumably functioning as a glandular evaporation apparatus, and the antennomere II subdivided into three sections, are suggested as synapomorphies of Mastigini; within Mastigitae this tribe is also unique in lacking the urogomphs, which are present in larvae of Leptomastacini and Clidicini. Geniculate and slender antennae with a strongly oblique distal margin of antennomere II are a putative larval synapomorphy of Mastigitae.

Gene expression profiles uncover individual identities of gnathal neuroblasts and serial homologies in the embryonic CNS of Drosophila.

The numbers and types of progeny cells generated by neural stem cells in the developing CNS are adapted to its region-specific functional requirements. In Drosophila, segmental units of the CNS develop from well-defined patterns of neuroblasts. Here we constructed comprehensive neuroblast maps for the three gnathal head segments. Based on the spatiotemporal pattern of neuroblast formation and the expression profiles of 46 marker genes (41 transcription factors), each neuroblast can be uniquely identified. Compared with the thoracic ground state, neuroblast numbers are progressively reduced in labial, maxillary and mandibular segments due to smaller sizes of neuroectodermal anlagen and, partially, to suppression of neuroblast formation and induction of programmed cell death by the Hox gene Deformed. Neuroblast patterns are further influenced by segmental modifications in dorsoventral and proneural gene expression. With the previously published neuroblast maps and those presented here for the gnathal region, all neuroectodermal neuroblasts building the CNS of the fly (ventral nerve cord and brain, except optic lobes) are now individually identified (in total 2×567 neuroblasts). This allows, for the first time, a comparison of the characteristics of segmental populations of stem cells and to screen for serially homologous neuroblasts throughout the CNS. We show that approximately half of the deutocerebral and all of the tritocerebral (posterior brain) and gnathal neuroblasts, but none of the protocerebral (anterior brain) neuroblasts, display serial homology to neuroblasts in thoracic/abdominal neuromeres. Modifications in the molecular signature of serially homologous neuroblasts are likely to determine the segment-specific characteristics of their lineages.

Redescription of late-instar larva of Scydmoraphes sparshalli (Denny)Coleoptera: Staphylinidae, Scydmaeninae).

The larva of Scydmoraphes sparshalli is redescribed. This is the first complete description of an immature Scydmoraphes with special focus on the chaetotaxic characters. The larva is unique among Cyrtoscydmini in having three pairs of stemmata, a very long sensory appendage of the antennomere II, mandibles with mesal row of microserrations interrupted by smooth portion of mandibular margin; maxillary mala with asetose apex and a row of very long, modified setae on mesal margin, and extremely elongate maxillary palpomere III and labium. A comparative study of previous descriptions resulted in recognizing a misidentification of a Scydmoraphes larva (the "Typ 2-Larve" of Schmid) as a putative Neuraphes (Pararaphes). The serial homology of chaetotaxic structures in the larva of Scydmoraphes sparshalli is discussed, and comparative notes on the larvae of Scydmoraphes, Neuraphes and Stenichnus are given, with an identification key.