Evolutionary Elaboration Research Articles

Anatomical, Ontogenetic, and Genomic Homologies Guide Reconstructions of the Teeth-to-Baleen Transition in Mysticete Whales

The transition in Mysticeti (Cetacea) from capture of individual prey using teeth to bulk filtering batches of small prey using baleen ranks among the most dramatic evolutionary transformations in mammalian history. We review phylogenetic work on the homology of mysticete feeding structures from anatomical, ontogenetic, and genomic perspectives. Six characters with key functional significance for filter-feeding behavior are mapped to cladograms based on 11 morphological datasets to reconstruct evolutionary change across the teeth-to-baleen transition. This comparative summary within a common parsimony framework reveals extensive conflicts among independent systematic efforts but also broad support for the newly named clade Kinetomenta (Aetiocetidae + Chaeomysticeti). Complementary anatomical studies using CT scans and ontogenetic series hint at commonalities between the developmental programs for teeth and baleen, lending further support for a 'transitional chimaeric feeder' scenario that best explains current evidence on the transition to filter feeding. For some extant mysticetes, the ontogenetic sequence in fetal specimens recapitulates the inferred evolutionary transformation: from teeth, to teeth and baleen, to just baleen. Phylogenetic mapping of inactivating mutations reveals mutational decay of ‘dental genes’ related to enamel formation before the emergence of crown Mysticeti, while ‘baleen genes’ that were repurposed or newly derived during the evolutionary elaboration of baleen currently are poorly characterized. Review and meta-analysis of available data suggest that the teeth-to-baleen transition in Mysticeti is one of the best characterized macroevolutionary shifts due to the diversity of data from the genome, the fossil record, comparative anatomy, and ontogeny that directly bears on this remarkable evolutionary transformation.

How cells tell up from down and stick together to construct multicellular tissues - interplay between apicobasal polarity and cell-cell adhesion.

Polarized epithelia define a topological inside and outside, and hence constitute a key evolutionary innovation that enabled the construction of complex multicellular animal life. Over time, this basic function has been elaborated upon to yield the complex architectures of many of the organs that make up the human body. The two processes necessary to yield a polarized epithelium, namely regulated adhesion between cells and the definition of the apicobasal (top-bottom) axis, have likewise undergone extensive evolutionary elaboration, resulting in multiple sophisticated protein complexes that contribute to both functions. Understanding how these components function in combination to yield the basic architecture of a polarized cell-cell junction remains a major challenge. In this Review, we introduce the main components of apicobasal polarity and cell-cell adhesion complexes, and outline what is known about their regulation and assembly in epithelia. In addition, we highlight studies that investigate the interdependence between these two networks. We conclude with an overview of strategies to address the largest and arguably most fundamental unresolved question in the field, namely how a polarized junction arises as the sum of its molecular parts.

Ancient origin of fucosylated xyloglucan in charophycean green algae

The charophycean green algae (CGA or basal streptophytes) are of particular evolutionary significance because their ancestors gave rise to land plants. One outstanding feature of these algae is that their cell walls exhibit remarkable similarities to those of land plants. Xyloglucan (XyG) is a major structural component of the cell walls of most land plants and was originally thought to be absent in CGA. This study presents evidence that XyG evolved in the CGA. This is based on a) the identification of orthologs of the genetic machinery to produce XyG, b) the identification of XyG in a range of CGA and, c) the structural elucidation of XyG, including uronic acid-containing XyG, in selected CGA. Most notably, XyG fucosylation, a feature considered as a late evolutionary elaboration of the basic XyG structure and orthologs to the corresponding biosynthetic enzymes are shown to be present in Mesotaenium caldariorum.

Foraging and feeding are independently regulated by social and personal hunger in the clonal raider ant

Ant colonies must assess the internal states of their members and coordinate their responses to changes in state. One important example of this is the sensing of colony hunger and the regulation of foraging behavior. In many ant species, workers’ own nutritional states at least partially determine how much they forage, and poorly nourished workers usually forage more, while well-nourished workers remain inside the nest. Workers in some species, such as the clonal raider ant Ooceraea biroi, mostly forage in response to larval signals. Here, we ask whether O. biroi larvae directly affect worker nutrition, and whether nutritional states in turn regulate workers’ foraging and feeding behavior. We find that larval signals do not detectably influence workers’ nutritional states or feeding behavior. Unlike in most other ant species, however, when colonies forage in response to larval signals, better-nourished O. biroi workers forage more. This suggests evolutionary modifications to the nature and strength of the relationship between nutritional state and foraging behavior in some ants. Nonetheless, worker nutritional states regulate feeding behavior as expected, with workers eating in proportion to their level of food deprivation. We discuss the implications of these results for the life history of O. biroi and the evolution of foraging regulation in social insects more generally. We suggest that the decoupling of regulatory mechanisms for feeding and foraging has parallels in the evolutionary elaboration of animal multicellularity. Foraging in social insects is a cooperative behavior: workers forage for the colony, rather than just for themselves. In most species, workers primarily use their own hunger as proxies for the colony’s needs. However, some species use other sources of information. Clonal raider ants, for example, forage in response to signals from their larvae. Here, we ask whether they also forage when deprived of nutrition. Surprisingly, we find instead that they forage more when better fed, and that in unmanipulated colonies, larval signals override worker nutrition, suggesting that the regulation of foraging has been rewired in this species. We also find that workers feed in proportion to their nutrient deprivation, suggesting that the regulation of feeding has been conserved. We propose that the uncoupling of feeding and foraging machinery has parallels in the evolutionary elaboration of animal multicellularity.

Dasykothon leptomiscus gen. et sp. nov., a fossil flower of possible Lauralean affinity from Myanmar amber

A new fossil angiosperm, Dasykothon leptomiscus, is described from mid-Cretaceous amber deposits in the Hukawng Valley of northwestern Myanmar (Burma). The flower is post-anthesis except for one stamen that retains its pollen. The perianth is slightly irregular and composed of 5 ovate or lance-linear, erect or incurved sepals. The ca. 12 stamens have slender, elongate filaments and dorsifixed, bithecal, longitudinally dehiscent anthers. The superior ovary bears 2 long, curved styles. Germinating pollen grains observed on the stigmas are monoporate and have the peculiar feature of a grooved ridge encircling the grain from pole to pole. This structure is hypothesized to be an evolutionary elaboration of the meridionally syncolpate sulcus found in some members of the Atherospermataceae. The generalized floral morphology of the fossil prevents ready taxonomic assignment to a modern family.

The making of elaborate petals in Nigella through developmental repatterning.

Elaborate petals are present in many flowering plants lineages and have greatly promoted the success and evolutionary radiation of these groups. How elaborate petals are made, however, remains largely unclear. Petals of Nigella (Ranunculaceae) have long been recognized as elaborate and can thus be an excellent model for the study of petal elaboration. Here, by conducting detailed morphological, micromorphological, anatomical, developmental and evolutionary studies on the petals of Nigella species, we explored the processes, general patterns and underlying mechanisms of petal elaboration. We found that petals of Nigella are highly complex, and the complexity can be reflected at various levels. We also found that evolutionary elaboration of the Nigella petals is a gradual process, involving not only modifications of pre-existing structures but also de novo origination of new characters. Further investigations indicated that the elaboration and diversification of Nigella petals were accomplished by modifying the ancestral trajectory of petal development, a process known as developmental repatterning. Our results not only provide new insights into the development and evolution of elaborate petals, but also highlight the necessity of conducting multiple-level investigations for understanding the processes, patterns and underlying mechanisms of plant evolution.

Structural and physical determinants of the proboscis\u2013sucking pump complex in the evolution of fluid-feeding insects

Fluid-feeding insects have evolved a unique strategy to distribute the labor between a liquid-acquisition device (proboscis) and a sucking pump. We theoretically examined physical constraints associated with coupling of the proboscis and sucking pump into a united functional organ. Classification of fluid feeders with respect to the mechanism of energy dissipation is given by using only two dimensionless parameters that depend on the length and diameter of the proboscis food canal, maximum expansion of the sucking pump chamber, and chamber size. Five species of Lepidoptera — White-headed prominent moth (Symmerista albifrons), White-dotted prominent moth (Nadata gibosa), Monarch butterfly (Danaus plexippus), Carolina sphinx moth (Manduca sexta), and Death’s head sphinx moth (Acherontia atropos) — were used to illustrate this classification. The results provide a rationale for categorizing fluid-feeding insects into two groups, depending on whether muscular energy is spent on moving fluid through the proboscis or through the pump. These findings are relevant to understanding energetic costs of evolutionary elaboration and reduction of the mouthparts and insect diversification through development of new habits by fluid-feeding insects in general and by Lepidoptera in particular.

Resource allocation during ontogeny is influenced by genetic, developmental and ecological factors in the horned beetle, Onthophagus taurus.

Resource allocation trade-offs arise when developing organs are in competition for a limited pool of resources to sustain growth and differentiation. Such competition may constrain the maximal size to which structures can grow and may force a situation in which the evolutionary elaboration of one structure may only be possible at the expense of another. However, recent studies have called into question both the consistency and evolutionary importance of resource allocation trade-offs. This study focuses on a well-described trade-off between the horns and eyes of Onthophagus beetles and assesses the degree to which it is influenced by genetic, developmental and ecological conditions. Contrary to expectations, we observed that trade-off signatures (i) were mostly absent within natural populations, (ii) mostly failed to match naturally evolved divergences in horn investment among populations, (iii) were subject to differential changes in F1 populations derived from divergent field populations and (iv) remained largely unaffected by developmental genetic manipulations of horn investment. Collectively, our results demonstrate that populations subject to different ecological conditions exhibit different patterns of, and differential plasticity in, resource allocation. Further, variation in ecological conditions, rather than canalized developmental mechanisms, may determine whether and to what degree morphological structures engage in resource allocation trade-offs.

Pattern and polarity in the development and evolution of the gnathostome jaw: Both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula

The acquisition of jaws constitutes a landmark event in vertebrate evolution, one that in large part potentiated their success and diversification. Jaw development and patterning involves an intricate spatiotemporal series of reciprocal inductive and responsive interactions between the cephalic epithelia and the cranial neural crest (CNC) and cephalic mesodermal mesenchyme. The coordinated regulation of these interactions is critical for both the ontogenetic registration of the jaws and the evolutionary elaboration of variable jaw morphologies and designs. Current models of jaw development and evolution have been built on molecular and cellular evidence gathered mostly in amniotes such as mice, chicks and humans, and augmented by a much smaller body of work on the zebrafish. These have been partnered by essential work attempting to understand the origins of jaws that has focused on the jawless lamprey. Chondrichthyans (cartilaginous fish) are the most distant group to amniotes within extant gnathostomes, and comprise the crucial clade uniting amniotes and agnathans; yet despite their critical phylogenetic position, evidence of the molecular and cellular underpinnings of jaw development in chondrichthyans is still lacking. Recent advances in genome and molecular developmental biology of the lesser spotted dogfish shark, Scyliorhinus canicula, make it ideal for the molecular study of chondrichthyan jaw development. Here, following the ‘Hinge and Caps' model of jaw development, we have investigated evidence of heterotopic (relative changes in position) and heterochronic (relative changes in timing) shifts in gene expression, relative to amniotes, in the jaw primordia of S. canicula embryos. We demonstrate the presence of clear proximo-distal polarity in gene expression patterns in the shark embryo, thus establishing a baseline molecular baüplan for branchial arch-derived jaw development and further validating the utility of the ‘Hinge and Caps’ model in comparative studies of jaw development and evolution. Moreover, we correlate gene expression patterns with the absence of a lambdoidal junction (formed where the maxillary first arch meets the frontonasal processes) in chondrichthyans, further highlighting the importance of this region for the development and evolution of jaw structure in advanced gnathostomes.

A Neuronal Network Switch for Approach/Avoidance Toggled by Appetitive State

Concrete examples of computation and implementation of cost/benefit decisions at the level of neuronal circuits are largely lacking. Such decisions are based on appetitive state, which is the integration of sensation, internal state, and memory. Value-based decisions are accessible in neuronal circuitry of simple systems. In one such system, the predatory sea slug Pleurobranchaea, appetite is readily quantified in behavior and related to approach/avoidance decision. Moreover, motor aspects of feeding and turning can be observed as fictive motor output in the isolated central nervous system (CNS). Here we found that the excitation state of the feeding motor network both manifested appetitive state and controlled expression of orienting versus avoidance. In isolated CNSs, spontaneous feeding network activity varied proportionally to donor feeding thresholds. CNSs from low- and high-feeding-threshold donors expressed fictive orienting or avoidance, respectively, in response to brief stimulation of sensory nerves. Artificially exciting the feeding network converted fictive avoidance to orienting. Thus, the feeding network embodied appetitive state and toggled approach/avoidance decision by configuring response symmetry of the premotor turn network. A resulting model suggests a basic cost/benefit decision module from which to consider evolutionary elaboration of the circuitry to serve more intricate valuation processes in complex animals.

It's All Life History

It's All Life History

Structural evidence why males of Panorpa liui offer prey rather than salivary mass as their nuptial gift

AbstractMa, N. and Hua, B. 2011. Structural evidence why males ofPanorpa liuiofferprey rather than salivary mass as their nuptial gift. —Acta Zoologica(Stockholm)92: 398–403.The scorpionflies are considered as ideal model animals for the study of matingsystems in insects. The males generally offer both prey and salivary mass asnuptial gifts to the females during copulation. Our field observations show thatPanorpa liuiis peculiar because the males offer only prey rather than salivarysecretions as nuptial gift. Through anatomical and histological examinations, thesalivary glands ofP. liuiwere found to be devoid of sexual dimorphism inPano-rpa for the first time. Both the male and femaleP. liui bear simple salivaryglands, which are only composed of a common duct and two short sac-likeglands. This is the first attempt to explore the relationship between the salivaryglands and the mating tactics from the structural aspect inPanorpa, speculatingthat the simple structure of the male salivary glands inP. liuimight be responsi-ble for its failing to produce salivary mass as a nuptial gift during copulation.Compared with Boreidae, Meropidae, Bittacidae and Panorpidae, we presumethat the absence of sexual dimorphism ofthe salivary glands might represent aplesiomorphy inP. liui. The origin and evolutionary process of the nuptial giftbehaviour are tentatively speculated inPanorpa.Baozhen Hua, Entomological Museum, Northwest AF Engqvist and Sauer2001). Most of the recent studies have related to the selectivepressures responsible for the maintenance or behind the evo-lutionary elaboration of nuptial gifts (Vahed 1998).The scorpionflies in the genusPanorpa(Mecoptera: Pano-rpidae) are relatively weak flyers, only feeding upon soft-bod-ied dead arthropods (mainly insects) as scavengers (Byers andThornhill 1983), and have been used as model animals for thestudy of insect mating system (Carpenter 1931; Thornhill1981; Byers and Thornhill 1983; Engqvist and Sauer 2003).In general, male scorpionflies may obtain mating in threealternative ways, offering salivary masses, offering prey giftsor copulations with no gifts (Thornhill 1981; Byers andThornhill 1983). Generally, the third alternative is forceful,but in some European species copulation without gifts maytake place without force when the food resource is limited(Engqvist and Sauer 2003). In the males ofPanorpa, bothnuptial preys and salivary masses are used as mating effort toentice females to copulate. Females discriminate against malesthat are unable to produce salivary masses and⁄or to offer adead arthropod (Thornhill 1981; Bockwinkel and Sauer1994). Nuptial gifts inPanorpa also function to maximizeejaculate transfer. The duration of copulation is considerablylonger for the males that offer nuptial gifts (Bockwinkel andSauer 1994) and is also positively related to the number of sal-ivary masses provided by a male (Thornhill 1981; Thornhilland Sauer 1991; Saueret al.1998).

Evolutionary elaboration of interneuronal diversity: Relevance for human cognitive disorders.

Evolutionary elaboration of interneuronal diversity: Relevance for human cognitive disorders.

Consciousness as Recursive, Spatiotemporal Self-Location

AbstractAt the phenomenal level, consciousness can be described as a singular, unified field of recursive self-awareness, consistently coherent in a particular way; that of a subject located both spatially and temporally in an egocentrically-extended domain, such that conscious self-awareness is explicitly characterized by I-ness, now-ness and here-ness. The psychological mechanism underwriting this spatiotemporal self-locatedness and its recursive processing style involves an evolutionary elaboration of the basic orientative reference frame which consistently structures ongoing spatiotemporal self-location computations as i-here-now. Cognition computes action-output in the midst of ongoing movement, and consequently requires a constant self-locating spatiotemporal reference frame as basis for these computations. Over time, constant evolutionary pressures for energy efficiency have encouraged both the proliferation of anticipative feedforward processing mechansims, and the elaboration, at the apex of the sensorimotor processing hierarchy, of self-activating, highly attenuated recursively-feedforward circuitry processing the basic orientational schema independent of external action output. As the primary reference frame of active waking cognition, this recursive i-here-now processing generates a zone of subjective self-awareness in terms of which it feels like something to be oneself here and now. This is consciousness.

Consciousness as Recursive, Spatiotemporal Self-Location

At the phenomenal level, consciousness can be described as a singular, unified field of recursive self-awareness, consistently coherent in a particular way; that of a subject located both spatially and temporally in an egocentrically-extended domain, such that conscious self-awareness is explicitly characterized by I-ness, now-ness and here-ness. The psychological mechanism underwriting this spatiotemporal self-locatedness and its recursive processing style involves an evolutionary elaboration of the basic orientative reference frame which consistently structures ongoing spatiotemporal self-location computations as i-here-now. Cognition computes action-output in the midst of ongoing movement, and consequently requires a constant self-locating spatiotemporal reference frame as basis for these computations. Over time, constant evolutionary pressures for energy efficiency have encouraged both the proliferation of anticipative feedforward processing mechansims, and the elaboration, at the apex of the sensorimotor processing hierarchy, of self-activating, highly attenuated recursively-feedforward circuitry processing the basic orientational schema independent of external action output. As the primary reference frame of active waking cognition, this recursive i-here-now processing generates a zone of subjective self-awareness in terms of which it feels like something to be oneself here and now. This is consciousness.

Consciousness as recursive, spatiotemporal self-location

At the phenomenal level, consciousness arises in a consistently coherent fashion as a singular, unified field of recursive self-awareness (subjectivity) with explicitly orientational characteristics--that of a subject located both spatially and temporally in an egocentrically-extended domain. Understanding these twin elements of consciousness begins with the recognition that ultimately (and most primitively), cognitive systems serve the biological self-regulatory regime in which they subsist. The psychological structures supporting self-located subjectivity involve an evolutionary elaboration of the two basic elements necessary for extending self-regulation into behavioral interaction with the environment: an orientative reference frame which consistently structures ongoing interaction in terms of controllable spatiotemporal parameters, and processing architecture that relates behavior to homeostatic needs via feedback. Over time, constant evolutionary pressures for energy efficiency have encouraged the emergence of anticipative feedforward processing mechanisms, and the elaboration, at the apex of the sensorimotor processing hierarchy, of self-activating, highly attenuated recursively-feedforward circuitry processing the basic orientational schema independent of external action output. As the primary reference frame of active waking cognition, this recursive self-locational schema processing generates a zone of subjective self-awareness in terms of which it feels like something to be oneself here and now. This is consciousness-as-subjectivity.

Consciousness as Recursive, Spatiotemporal Self-Location

AbstractAt the phenomenal level, consciousness can be described as a singular, unified field of recursive self-awareness, consistently coherent in a particular way; that of a subject located both spatially and temporally in an egocentrically-extended domain, such that conscious self-awareness is explicitly characterized by I-ness, now-ness and here-ness. The psychological mechanism underwriting this spatiotemporal self-locatedness and its recursive processing style involves an evolutionary elaboration of the basic orientative reference frame which consistently structures ongoing spatiotemporal self-location computations as i-here-now. Cognition computes action-output in the midst of ongoing movement, and consequently requires a constant self-locating spatiotemporal reference frame as basis for these computations. Over time, constant evolutionary pressures for energy efficiency have encouraged both the proliferation of anticipative feedforward processing mechansims, and the elaboration, at the apex of the sensorimotor processing hierarchy, of self-activating, highly attenuated recursively-feedforward circuitry processing the basic orientational schema independent of external action output. As the primary reference frame of active waking cognition, this recursive i-here-now processing generates a zone of subjective self-awareness in terms of which it feels like something to be oneself here and now. This is consciousness.

Evolvability and Robustness in Color Displays: Bridging the Gap between Theory and Data

Evolution of diet-derived sexual orna- ments—some of the most spectacular and diverse traits in the living world—highlights the gap between modern evo- lutionary theory and empirical data on the origin and inheritance of complex environment-dependent traits. Spe- cifically, current theory offers little insight into how strong environmental contingency of diet-dependent color bio- synthesis and environmental variability in precursor supply can be reconciled with extensive evolutionary elaboration, diversification, and convergence of diet-dependent displays among animal taxa. Moreover, biosynthetic pathways of diet-derived displays combine seemingly irreconcilable robustness, lability, and modularity to facilitate elaboration under variable environmental conditions. Here I show that an ontogenetic decrease in the predictability of an associa- tion between organismal and environmental components of color biosynthesis and the corresponding evolutionary transition from short-term epigenetic inheritance of peripheral biosynthetic components to genetic inheritance of the most reliable upstream components link the causes of developmental variation with the causes of inheritance in diet-derived displays. Using carotenoid-based colors as an empirical model, I outline general principles of a testable evolutionary framework of diversification and functional robustness of diet-derived displays, and suggest that such a framework provides insight into the foundational question of evolutionary biology—how to connect causes of within- generation developmental variation with causes of among- generation and among-taxa variation and thus with causes of evolution?

Coevolution between harmful male genitalia and female resistance in seed beetles

Reproductive conflict between the sexes is thought to be a key force in the evolution of many reproductive characters, but persuasive evidence for its significance is still scarce. The spectacular evolution of male genitalia that impose physical injury on females during mating has often been suggested to be a product of sexually antagonistic coevolution, but our understanding of these extraordinary adaptations is very limited, and there are no direct data addressing their evolutionary elaboration. We show that more spiny male genitalia causes more harm to females during copulation and provide comparative evidence for the correlated evolution between these antagonistic adaptations in males and a female counteradaptation (the amount of connective tissue in the copulatory duct) in a group of insects. By combining comparative and experimental methods, we demonstrate that imbalance of relative armament of the sexes affects evolution of the economics of reproduction: as males evolve genitalia that are more harmful relative to the level of female counteradaptation, costs associated with mating for females increase and population fitness is depressed. Our results unveil a coevolutionary arms race between the sexes and are consistent with a proposed link between sexual conflict, species' viability, and the risk of extinction.

Social complexity in bees is not sufficient to explain lack of reversions to solitary living over long time scales

BackgroundThe major lineages of eusocial insects, the ants, termites, stingless bees, honeybees and vespid wasps, all have ancient origins (≥ 65 mya) with no reversions to solitary behaviour. This has prompted the notion of a 'point of no return' whereby the evolutionary elaboration and integration of behavioural, genetic and morphological traits over a very long period of time leads to a situation where reversion to solitary living is no longer an evolutionary option.ResultsWe show that in another group of social insects, the allodapine bees, there was a single origin of sociality > 40 mya. We also provide data on the biology of a key allodapine species, Halterapis nigrinervis, showing that it is truly social. H. nigrinervis was thought to be the only allodapine that was not social, and our findings therefore indicate that there have been no losses of sociality among extant allodapine clades. Allodapine colony sizes rarely exceed 10 females per nest and all females in virtually all species are capable of nesting and reproducing independently, so these bees clearly do not fit the 'point of no return' concept.ConclusionWe argue that allodapine sociality has been maintained by ecological constraints and the benefits of alloparental care, as opposed to behavioural, genetic or morphological constraints to independent living. Allodapine brood are highly vulnerable to predation because they are progressively reared in an open nest (not in sealed brood cells), which provides potentially large benefits for alloparental care and incentives for reproductives to tolerate potential alloparents. We argue that similar vulnerabilities may also help explain the lack of reversions to solitary living in other taxa with ancient social origins.