Evolutionary Precursor Research Articles

Identification of a signature of evolutionarily conserved stress-induced mutagenesis in cancer.

The clustering of mutations observed in cancer cells is reminiscent of the stress-induced mutagenesis (SIM) response in bacteria. Bacteria deploy SIM when faced with DNA double-strand breaks in the presence of conditions that elicit an SOS response. SIM employs DinB, the evolutionary precursor to human trans-lesion synthesis (TLS) error-prone polymerases, and results in mutations concentrated around DNA double-strand breaks with an abundance that decays with distance. We performed a quantitative study on single nucleotide variant calls for whole-genome sequencing data from 1950 tumors, non-inherited mutations from 129 normal samples, and acquired mutations in 3 cell line models of stress-induced adaptive mutation. We introduce statistical methods to identify mutational clusters, quantify their shapes and tease out the potential mechanism that produced them. Our results show that mutations in both normal and cancer samples are indeed clustered and have shapes indicative of SIM. Clusters in normal samples occur more often in the same genomic location across samples than in cancer suggesting loss of regulation over the mutational process during carcinogenesis. Additionally, the signatures of TLS contribute the most to mutational cluster formation in both patient samples as well as experimental models of SIM. Furthermore, a measure of cluster shape heterogeneity was associated with cancer patient survival with a hazard ratio of 5.744 (Cox Proportional Hazard Regression, 95% CI: 1.824–18.09). Our results support the conclusion that the ancient and evolutionary-conserved adaptive mutation response found in bacteria is a source of genomic instability in cancer. Biological adaptation through SIM might explain the ability of tumors to evolve in the face of strong selective pressures such as treatment and suggests that the conventional ‘hit it hard’ approaches to therapy could prove themselves counterproductive.

Laughter, bonding and biological evolution

This paper combines perspectives from evolutionary biology and linguistics to discuss the early evolution of laughter and the possible role of laughter-like vocalisation as a bonding mechanism in hominins and early human species. From the perspective of evolutionary biology, we here emphasise several things: the role of exaptation, the typically very slow pace of evolutionary change, and the danger of projecting backwards from the current utilities of laughter to infer its earlier function, hundreds of thousands, or even millions, of years ago. From the perspective of linguistics, we examine both the semantics of the word ‘laugh’ and the vocal mechanics of human laughter production, arguing that greater terminological care is needed in talking about the precursors of laughter in the ancient evolutionary past. Finally, we turn to hypotheses about how laughter-like vocalisations may have arisen, long before articulate language as we know it today. We focus in particular on Robin Dunbar’s hypothesis that laughter-like vocalisation, which stimulated endorphin production, might have functioned as a bonding mechanism (a kind of “vocal grooming”) among hominins and early human species. The paper contributes to the special issue theme (Humour and Belonging) by casting a long look backwards in time to laughter-like vocalisation as a distant evolutionary precursor of humour, and to bonding as an evolutionary precursor to cognitively and socially modern forms of “belonging”. At the same time, it cautions against casual theorising about the evolutionary origins of laughter.

B cell selection sites in the nurse shark spleen may represent evolutionary precursors of mammalian germinal centers

Abstract Sharks are members of the oldest extant taxonomic group (Chondrichthyes) to have immunoglobulin (Ig)-based adaptive immunity. While research has demonstrated that sharks can produce antigen-specific antibody responses, affinity mature these antibodies, and establish immunological memory, histological examination has so far failed to find evidence of germinal centers (GCs). To explore this apparent discrepancy, we immunized several nurse sharks (Ginglymostoma cirratum) with phycoerythrin and visualized the subsequent splenic response using a combination of single nuclei (sn)RNA sequencing and fluorescent microscopy. Our snRNA data reveal the presence of both centrocyte-like and centroblast-like B cells in sharks, as well as a T cell subset expressing several markers found in mammalian T follicular helper cells. RNA fluorescent in situ hybridization experiments show distinct regions of AID expression, polarization of CXCR4 and CXCR5 expression, and association of T cell aggregates with splenic B cell follicles. Fluorescent microscopy clearly demonstrates presentation of nondegraded antigen in the center of B cell follicles. Finally, analysis of Ig variable regions amplified from such B cell follicles reveals evidence of positive selection of clonotypes. Together, our data supports the presence of B cell selection sites in the cartilaginous fish spleen that functionally support the selection of antigen-specific B cells and affinity maturation of the shark Ig repertoire. Further, these sites potentially represent the primordial structures that gave rise to mammalian GCs. Supported by grants from NIH T32 AI095190, F31 AI147532

Aggregation of IgM+, TCRβ+ and CD4+ Cells around melanomacrophage centers - evidence of an organized lymphoid structure in a teleost

Abstract The study of immunity in non-model organisms has the potential to reveal the evolved diversity of the immune system. However, such studies are hampered by the paucity of species-specific reagents. Advances in single-molecule RNA-ISH overcomes these setbacks and allows for the detection of potentially dozens of gene targets in a single tissue section. We examined the spatial expression of immune genes in the splenic tissue of a teleost, threespine stickleback, using the advanced multiplexed RNAScope Hiplex assay. Threespine stickleback, a small teleost found throughout the Northern Hemisphere, is an emerging immunologic model. It has been proposed that teleost humoral adaptive immunity initiates in the melanomacrophage center (MMC), a putative evolutionary precursor to germinal centers (GC), however this has not been directly tested. Teleosts lack GCs, yet still generate affinity matured antibodies in response to antigen challenge. We find that stickleback MMCs increase in size in response to antigen immunization but not to control injection, suggesting that MMC response is antigen driven, similar to the mammalian GC. Analysis of splenic tissue indicates that IgM mRNA expressing cells aggregate in discrete regions around stickleback MMCs. Similarly, CD4 and TCR-β expressing cells aggregate near IgM+ cells, comparable to the organization of B and T cells in mammalian GCs. These findings suggest that stickleback splenic tissues have an organized structure, focused around the MMCs, and support the hypothesis that MMCs could be the site of teleost adaptive immunity and the evolutionary precursors to GCs. This study also highlights the application of RNAScope in a non-model organism. Supported by NIH RO1AI146168

Structural and Biophysical Analysis of the Phytochelatin-Synthase-Like Enzyme from Nostoc sp. Shows That Its Protease Activity is Sensitive to the Redox State of the Substrate.

Phytochelatins (PCs) are nonribosomal thiol-rich oligopeptides synthetized from glutathione (GSH) in a γ-glutamylcysteinyl transpeptidation reaction catalyzed by PC synthases (PCSs). Ubiquitous in plant and present in some invertebrates, PCSs are involved in metal detoxification and homeostasis. The PCS-like enzyme from the cyanobacterium Nostoc sp. (NsPCS) is considered to be an evolutionary precursor enzyme of genuine PCSs because it shows sufficient sequence similarity for homology to the catalytic domain of the eukaryotic PCSs and shares the peptidase activity consisting in the deglycination of GSH. In this work, we investigate the catalytic mechanism of NsPCS by combining structural, spectroscopic, thermodynamic, and theoretical techniques. We report several crystal structures of NsPCS capturing different states of the catalyzed chemical reaction: (i) the structure of the wild-type enzyme (wt-NsPCS); (ii) the high-resolution structure of the γ-glutamyl-cysteine acyl-enzyme intermediate (acyl-NsPCS); and (iii) the structure of an inactive variant of NsPCS, with the catalytic cysteine mutated into serine (C70S-NsPCS). We characterize NsPCS as a relatively slow enzyme whose activity is sensitive to the redox state of the substrate. Namely, NsPCS is active with reduced glutathione (GSH), but is inhibited by oxidized glutathione (GSSG) because the cleavage product is not released from the enzyme. Our biophysical analysis led us to suggest that the biological function of NsPCS is being a part of a redox sensing system. In addition, we propose a mechanism how PCS-like enzymes may have evolved toward genuine PCS enzymes.

On the hybrid origin of the C2 Salsola divaricata agg. (Amaranthaceae) from C3 and C4 parental lineages.

C2 photosynthesis is characterised using recapturing photorespiratory CO2 by RuBisCo in Kranz-like cells and is therefore physiologically intermediate between C3 and C4 photosynthesis. C2 can be interpreted as an evolutionary precursor of C4 and/or as the result of hybridisation between a C3 and C4 lineage. We compared the expression of photosynthetic traits among populations of the Salsola divaricata agg. (C2 ) from humid subtropical to arid habitats on the coasts of the Canary Islands and Morocco and subjected them to salt and drought treatments. We screened for enhanced C4 -like expression of traits related to habitat or treatment. We estimated species trees with a transcriptome dataset of Salsoleae and explored patterns of gene tree discordance. With phylogenetic networks and hybridisation analyses we tested for the hybrid origin of the Salsola divaricata agg. We observed distinct independent variation of photosynthetic traits within and among populations and no clear evidence for selection towards C4 -like trait expression in more stressful habitats or treatments. We found reticulation and gene tree incongruence in Salsoleae supporting a putative hybrid origin of the Salsola divaricata agg. C2 photosynthesis in the Salsola divaricata agg. combines traits inherited from its C3 and C4 parental lineages and seems evolutionarily stable, possibly well adapted to a wide climatic amplitude.

Thyroid and endostyle development in cyclostomes provides new insights into the evolutionary history of vertebrates

BackgroundThe endostyle is an epithelial exocrine gland found in non-vertebrate chordates (amphioxi and tunicates) and the larvae of modern lampreys. It is generally considered to be an evolutionary precursor of the thyroid gland of vertebrates. Transformation of the endostyle into the thyroid gland during the metamorphosis of lampreys is thus deemed to be a recapitulation of a past event in vertebrate evolution. In 1906, Stockard reported that the thyroid gland in hagfish, the sister cyclostome group of lampreys, develops through an endostyle-like primordium, strongly supporting the plesiomorphy of the lamprey endostyle. However, the findings in hagfish thyroid development were solely based on this single study, and these have not been confirmed by modern molecular, genetic, and morphological data pertaining to hagfish thyroid development over the last century.ResultsHere, we showed that the thyroid gland of hagfish undergoes direct development from the ventrorostral pharyngeal endoderm, where the previously described endostyle-like primordium was not found. The developmental pattern of the hagfish thyroid, including histological features and regulatory gene expression profiles, closely resembles that found in modern jawed vertebrates (gnathostomes). Meanwhile, as opposed to gnathostomes but similar to non-vertebrate chordates, lamprey and hagfish share a broad expression domain of Nkx2-1/2-4, a key regulatory gene, in the pharyngeal epithelium during early developmental stages.ConclusionsBased on the direct development of the thyroid gland both in hagfish and gnathostomes, and the shared expression profile of thyroid-related transcription factors in the cyclostomes, we challenge the plesiomorphic status of the lamprey endostyle and propose an alternative hypothesis where the lamprey endostyle could be obtained secondarily in crown lampreys.

Anatomic position determines oncogenic specificity in melanoma.

Oncogenic alterations to DNA are not transforming in all cellular contexts1,2. This may be due to pre-existing transcriptional programmes in the cell of origin. Here we define anatomic position as a major determinant of why cells respond to specific oncogenes. Cutaneous melanoma arises throughout the body, whereas the acral subtype arises on the palms of the hands, soles of the feet or under the nails3. We sequenced the DNA of cutaneous and acral melanomas from a large cohort of human patients and found a specific enrichment for BRAF mutations in cutaneous melanoma and enrichment for CRKL amplifications in acral melanoma. We modelled these changes in transgenic zebrafish models and found that CRKL-driven tumours formed predominantly in the fins of the fish. The fins are the evolutionary precursors to tetrapod limbs, indicating that melanocytes in these acral locations may be uniquely susceptible to CRKL. RNA profiling of these fin and limb melanocytes, when compared with body melanocytes, revealed a positional identity gene programme typified by posterior HOX13 genes. This positional gene programme synergized with CRKL to amplify insulin-like growth factor (IGF) signalling and drive tumours at acral sites. Abrogation of this CRKL-driven programme eliminated the anatomic specificity of acral melanoma. These data suggest that the anatomic position of the cell of origin endows it with a unique transcriptional state that makes it susceptible to only certain oncogenic insults.

Externalized memory in slime mould and the extended (non-neuronal) mind

The hypothesis of extended cognition (HEC) claims that the cognitive processes that materially realise thinking are sometimes partially constituted by entities that are located external to an agent’s body in its local environment. We show how proponents of HEC need not claim that an agent must have a central nervous system, or physically instantiate processes organised in such a way as to play a causal role equivalent to that of the brain if that agent is to be capable of cognition. Focusing on the case of spatial memory, we make our argument by taking a close look at the striking example of Physarum Polycephalum plasmodium (i.e., slime mould) which uses self-produced non-living extracellular slime trails to navigate its environment. We will argue that the use of externalized spatial memory by basal organisms like Physarum is an example of extended cognition. Moreover, it is a possible evolutionary precursor to the use of internal spatial memory and recall in animals thus demonstrating how extended cognition may have emerged early in evolutionary history.

A New Perspective on the Maillard Reaction and the Origin of Life

The Maillard reaction, a spontaneous 'one pot' reaction between amino acids and reducing sugars that occurs at low reactant concentrations and low temperatures, is a good candidate for having played a role in the origin of life on the Earth. In view of the probability that RNA and DNA were preceded by an evolutionary forerunner with a more straightforward prebiotic synthesis, it is a testament to the prescience of Oró and colleagues that, in 1975, they drew attention to the Maillard reaction, in particular evidence that melanoidin polymers (the end-product of the reaction) contain '…heterocyclic nitrogen compounds similar to the nitrogenous bases' (Nissenbaum in J Mol Evol 6:253-270, 1975). Indeed, reports of the Maillard reaction product, 2-Acetyl-6-(Hydroxymethyl)-5,6-Dihydro-4H-Pyridinone (AHDP), with a structure reminiscent of the pyrimidine nucleobase uracil, suggest the Maillard reaction might have played a key role in the synthesis of components of a proto-RNA polymer, with AHDP and two structurally related products predicted to be similar to uracil in the latter's ability to form non-standard base pair interactions. It is possible that the primary function of these interactions was to allow molecules such as AHDP to separate out of the prebiotic chemical clutter. If this were the case, catalysis, and coding-made possible by the polymerization of proto-nucleoside monomers into linear sequence strings-would have been evolving properties.

Chimpanzee facial gestures and the implications for the evolution of language

Great ape manual gestures are described as communicative, flexible, intentional, and goal-oriented. These gestures are thought to be an evolutionary pre-cursor to human language. Conversely, facial expressions are thought to be inflexible, automatic, and derived from emotion. However, great apes can make a wide range of movements with their faces, and they may possess the control needed to gesture with their faces as well as their hands. We examined whether chimpanzee facial expressions possess the four important gesture properties and how they compare to manual gestures. To do this, we quantified variables that have been previously described through largely qualitative means. Chimpanzee facial expressions met all four gesture criteria and performed remarkably similar to manual gestures. Facial gestures have implications for the evolution of language. If other mammals also show facial gestures, then the gestural origins of language may be much older than the human/great ape lineage.

Evolutionary origins of cooperative and communal breeding: Lessons from the crotophagine cuckoos

AbstractMost cooperatively breeding birds live in family groups, in which a breeding pair is assisted by genetically related “helpers” who do not reproduce. In some species, however, several breeding adults reproduce in a single nest and cooperatively provide parental care to the mixed brood of nestlings. Recent comparative analyses have convincingly argued that these two forms of sociality—family‐based helping and communal breeding—are distinct, since they differ in key respects and have apparently arisen along separate evolutionary trajectories. In this review, I first suggest that the similarities between these systems are also informative for understanding the evolution and persistence of cooperative societies. For example, many communal breeders also have non‐reproductive helpers, suggesting that similar selective pressures may help maintain both kin‐based helping and communal breeding despite their disparate origins. I next discuss hypotheses for the origins of communal breeding in the anis and allies (CrotophagaandGuira), a lineage of Neotropical cuckoos, focusing on the evolutionary and behavioral links between communal breeding and brood parasitism. Several traits that are ancestral to cuckoos, including rapid offspring development and the ability to lay large, indeterminate clutches, are implicated as evolutionary precursors of both strategies. Finally, I discuss recent research on alternative reproductive tactics in the greater ani (Crotophaga major), in which communal breeding, conspecific brood parasitism, and helping by both relatives and non‐relatives are common. The coexistence of all four behaviors within the same population provides a rare opportunity to dissect the costs and benefits of group living and parental care, and, ultimately, to examine the selective pressures favoring cooperation under varying degrees of genetic relatedness.

Controlling Tumor Regression about the Physiological System

It is proposed to study the mechanism of tumor regression from an evolutionary point of view. The proposal is based on the assumption that the evolutionary precursor of this mechanism is the resorption mechanism in sedentary modular invertebrates preparing for diapause in embryos. To understand how the tumor regression mechanism works, it is necessary to investigate the mechanism of resorption of these embryos in these invertebrates.

Morphological basis for maternal nutrient provision to embryos in the viviparous fish Ataeniobius toweri (Teleostei: Goodeidae).

In viviparous Mexican fishes of the family Goodeidae, embryos develop in the maternal ovarian lumen. They typically absorb maternal nutrients during gestation by means of "trophotaeniae," that is, specialized, elongated extensions of the hindgut that are exposed to the fluids, which occupy the ovarian lumen. The sole exception is Ataeniobius toweri, whose embryos lack trophotaeniae but are nevertheless matrotrophic. Thus, how its embryos obtain maternal nutrients is unclear. We studied a series of non-pregnant and pregnant ovaries of A. toweri using histology to identify the mechanism of maternal-embryo nutrient transfer. By early-gestation, embryos have depleted their yolk supplies. Yolks are released into the ovarian lumen and are ingested by the developing embryos, as shown by yolk material in their digestive tracts. The embryonic gut is lined by an epithelium consisting of columnar cells with apical microvilli, providing a means for nutrient absorption. Contrary to statements in the literature, embryos develop minuscule trophotaenial rudiments that extend slightly into the ovarian lumen. These structures are formed of an absorptive epithelium that overlies a vascular stroma, similar to the trophotaeniae of other goodeids. Through late gestation, vitellogenic follicles form and oocytes are discharged into the ovarian lumen, contributing to embryonic nutrition. Thus, histological evidence suggests that embryos chiefly obtain nutrients from ingestion of yolk and maternal secretions released into the ovarian lumen. This function possibly is supplemented by uptake via the small hindgut protrusions and other absorptive surfaces (e.g., the skin and the gill epithelium). Our observations are consistent with two evolutionary interpretations of the hindgut protrusions: (a) that they are rudimentary, evolutionary precursors of trophotaeniae formed by exteriorized hindgut; and (b) that they are vestigial remnants of trophotaeniae that were lost during a switch to a form of matrotrophy involving nutrient ingestion.

Structural basis for glucocorticoid receptor recognition of both unmodified and methylated binding sites, precursors of a modern recognition element

The most common form of DNA methylation involves the addition of a methyl group to a cytosine base in the context of a cytosine–phosphate–guanine (CpG) dinucleotide. Genomes from more primitive organisms are more abundant in CpG sites that, through the process of methylation, deamination and subsequent mutation to thymine–phosphate–guanine (TpG) sites, can produce new transcription factor binding sites. Here, we examined the evolutionary history of the over 36 000 glucocorticoid receptor (GR) consensus binding motifs in the human genome and identified a subset of them in regulatory regions that arose via a deamination and subsequent mutation event. GR can bind to both unmodified and methylated pre-GR binding sequences (GBSs) that contain a CpG site. Our structural analyses show that CpG methylation in a pre-GBS generates a favorable interaction with Arg447 mimicking that made with a TpG in a GBS. This methyl-specific recognition arose 420 million years ago and was conserved during the evolution of GR and likely helps fix the methylation on the relevant cytosines. Our study provides the first genetic, biochemical and structural evidence of high-affinity binding for the likely evolutionary precursor of extant TpG-containing GBS.

Heterothermy, body size, and locomotion as ecological predictors of migration in mammals

Abstract Migration is ubiquitous among animals and has evolved repeatedly and independently. Comparative studies of the evolutionary origins of migration in birds are widespread, but are lacking in mammals. Mammalian species have greater variation in functional traits that may be relevant for migration. Interspecific variation in migration behaviour is often attributed to mode of locomotion (i.e. running, swimming, and flying) and body size, but traits associated with the evolutionary precursor hypothesis, including geographic distribution, habitat, and diet, could also be important predictors of migration in mammals. Furthermore, mammals vary in thermoregulatory strategies and include many heterothermic species, providing an alternative strategy to avoid seasonal resource depletion. We tested the evolutionary precursor hypothesis for the evolution of migration in mammals and tested predictions linking migration to locomotion, body size, geographic distribution, habitat, diet, and thermoregulation. We compiled a dataset of 722 species from 27 mammalian orders and conducted a series of analyses using phylogenetically informed models. Swimming and flying mammals were more likely to migrate than running mammals, and larger species were more likely to migrate than smaller ones. However, heterothermy was common among small running mammals that were unlikely to migrate. High‐latitude swimming and flying mammals were more likely to migrate than high‐latitude running mammals (where heterothermy was common), and most migratory running mammals were herbivorous. Running mammals and frugivorous bats with high thermoregulatory scope (greater capacity for heterothermy) were less likely to migrate, while insectivorous bats with high thermoregulatory scope were more likely to migrate. Our results indicate a broad range of factors that influence migration, depending on locomotion, body size, and thermoregulation. Our analysis of migration in mammals provided insight into some of the general rules of migration, and we highlight opportunities for future investigations of exceptions to these rules, ultimately leading to a comprehensive understanding of the evolution of migration.

Nest sanitation behavior does not increase the likelihood of parasitic egg rejection in herring gulls.

Birds’ behavioral response to brood parasitism can be influenced not only by evolution but also by context and individual experience. This could include nest sanitation, in which birds remove debris from their nests. Ultimately, nest sanitation behavior might be an evolutionary precursor to the rejection of parasitic eggs. Proximately, the context or experience of performing nest sanitation behavior might increase the detection or prime the removal of parasitic eggs, but evidence to date is limited. We tested incubation-stage nests of herring gulls Larus argentatus to ask whether nest sanitation increased parasitic egg rejection. In an initial set of 160 single-object experiments, small, red, blocky objects were usually rejected (18 of 20 nests), whereas life-sized, 3D-printed herring gull eggs were not rejected whether red (0 of 20) or the olive-tan base color of herring gull eggs (0 of 20). Next, we simultaneously presented a red, 3D-printed gull egg and a small, red block. These nests exhibited frequent nest sanitation (small, red block removed at 40 of 48 nests), but egg rejection remained uncommon (5 of those 40) and not significantly different from control nests (5 of 49) which received the parasitic egg but not the priming object. Thus, performance of nest sanitation did not shape individuals’ responses to parasitism. Interestingly, parents were more likely to reject the parasitic egg when they were present as we approached the nest to add the experimental objects. Depending on the underlying mechanism, this could also be a case of experience creating variation in responses to parasitism.

Bacterial Evolutionary Precursors of Eukaryotic Copper-Zinc Superoxide Dismutases.

Internalization of a bacteria by an archaeal cell expedited eukaryotic evolution. An important feature of the species that diversified into the great variety of eukaryotic life visible today was the ability to combat oxidative stress with a copper–zinc superoxide dismutase (CuZnSOD) enzyme activated by a specific, high-affinity copper chaperone. Adoption of a single protein interface that facilitates homodimerization and heterodimerization was essential; however, its evolution has been difficult to rationalize given the structural differences between bacterial and eukaryotic enzymes. In contrast, no consistent strategy for the maturation of periplasmic bacterial CuZnSODs has emerged. Here, 34 CuZnSODs are described that closely resemble the eukaryotic form but originate predominantly from aquatic bacteria. Crystal structures of a Bacteroidetes bacterium CuZnSOD portray both prokaryotic and eukaryotic characteristics and propose a mechanism for self-catalyzed disulfide maturation. Unification of a bacterial but eukaryotic-like CuZnSOD along with a ferredoxin-fold MXCXXC copper-binding domain within a single polypeptide created the advanced copper delivery system for CuZnSODs exemplified by the human copper chaperone for superoxide dismutase-1. The development of this system facilitated evolution of large and compartmentalized cells following endosymbiotic eukaryogenesis.

Proteomics analysis of the secondary hair follicle cycle in Liaoning cashmere goat

Cashmere is an important economic resource for the agricultural industry. The secondary hair follicle cycle can control the yield and quality of cashmere. Therefore, to improve the yield and quality of cashmere in Liaoning cashmere goats, an understanding of the skin proteomic changes in the secondary hair follicle cycle is needed. In this study, we used a label-free proteomics approach to analyze the protein expression profile of the secondary hair follicle cycle at three stages (telogen, anagen, and catagen) in goat neck skin. Proteomics, bioinformatics, and immunofluorescence assays were employed. We identified 57 differentially abundant proteins (DAPs) and discovered that the proteins of the keratin family were highly expressed in the anagen and catagen phases. The analyses indicated that nine keratin proteins (KRT25, KRT27, KRT19, KRT10, KRT77, KRT1, KRT24, KRT14, and KRT4) can be regarded as markers of the hair follicle cycle. KRT1 was located in both the inner and outer root sheath, whereas KRT14 was located in the inner root sheath and KRT19 only in the outer sheath. Phylogenetic analysis showed that these nine keratin proteins have common evolutionary precursors, and each category has similar expression patterns. Functional enrichment analysis indicated that the estrogen and ECM-receptor interaction signaling pathways play important roles in secondary hair follicle phases/cycles. These findings provide an important resource for protein information related to cashmere goats, and the identified DAPs can be further applied to improve cashmere quality and production.

Conditional valuation for combinations of goods in primates.

Valuing goods and selecting the one with the highest value forms the basis of adaptive behaviour across species. While it is obvious that the valuation of a given type of goods depends on ownership and availability of that type of goods, the effects of other goods on valuation of the original good are sometimes underappreciated. Yet, goods interact with each other, indicating that the valuation of a given good is conditional on the other goods it is combined with, both in the wild and the laboratory. Here, we introduce conditional valuation in the context of valuing multiple goods and briefly review how human and animal experimentalists can leverage economic tools for the study of interactions among goods. We then review evidence for conditional valuation for combined foods in both human and non-human primates. In the laboratory, non-human primates show increased valuation of certain combinations of foods but decreased valuation of other types of combinations. Thus, similarly to humans, monkeys appear to value combinations of goods in a conditional fashion. Additionally, both humans and monkeys appear to employ similar neural substrates for the valuation of single goods, such as the orbitofrontal cortex. Together, investigations of our evolutionary precursors may provide insights on how we value interacting goods. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.