Weiming Li

• Ph. D
• Chair at Michigan State University

Acrossocheilus fasciatus is a stream-dwelling fish species of the Barbinae subfamily. It is valued for its colorfully striped appearance and delicious meat. This species is also characterized by apparent sexual dimorphism and toxic ovum. Biology and aquaculture researches of A. fasciatus are hindered by the lack of a high-quality reference genome....

The sensory trap model of signal evolution suggests that males manipulate females into mating using traits that mimic cues used in a nonsexual context. Despite much empirical support for sensory traps, little is known about how females evolve in response to these deceptive signals. Female sea lamprey (Petromyzon marinus) evolved to discriminate a m...

The evolutionary origins of sexual preferences for chemical signals remain poorly understood, due, in part, to scant information on the molecules involved. In the current study, we identified a male pheromone in lake char (Salvelinus namaycush) to evaluate the hypothesis that it exploits a non-sexual preference for juvenile odour. In anadromous cha...

Thyroid hormones (TH) are known to play an important role in the growth and development of vertebrates. In fish species, TH regulates the larval-juvenile metamorphosis, and is crucial for development during early life stages. Monitoring the variations in TH levels at different life stages can provide insights into the regulation of metamorphosis an...

Toll-like receptors (TLRs) play an important role in innate immunity of defense against bacterial or viral pathogens. To study the biological characteristics and functions of the TLR genes, TLR14d was identified from Northeast Chinese lamprey (Lethenteron morii) and named LmTLR14d. LmTLR14d coding sequence (cds) is 3285 bp in length and encodes 109...

Introduction Adult sea lamprey (Petromyzon marinus) cease feeding and migrate to spawning streams where males build nests, undergo final sexual maturation, and subsequently produce and release large quantities of bile acid pheromones that attract mature females. These animals are predicted to rearrange their metabolic pathways drastically to suppor...

Reintroduction programs are important tools for wildlife conservation. However, captive rearing environments may lead to maladaptive behavior and physiological alterations that reduce survival probability after release. For captive rearing programs that raise individuals captured from the wild during early ontogeny for later release, there is a lac...

Introduction Adult sea lamprey (Petromyzon marinus) cease feeding and migrate to spawning streams where males build nests, undergo final sexual maturation, and subsequently produce and release large quantities of bile acid pheromones that attract mature females. These animals are predicted to rearrange their metabolic pathways drastically to suppor...

Per‐ and polyfluoroalkyl substances (PFAS) are contaminants of concern due to their widespread occurrence in the environment, persistence, and potential to elicit a range of negative health effects. PFAS are regularly detected in surface waters, but their effects on many aquatic organisms are still poorly understood. Species with thyroid‐dependent...

Costs to producing sexual signals can create selective pressures on males to invest signaling effort in particular contexts. When the benefits of signaling vary consistently across time, males can optimize signal investment to specific temporal contexts using biological rhythms. Sea lamprey, Petromyzon marinus, have a semelparous life history, are...

Biogenic amines activate G-protein coupled receptors (GPCRs) in the central nervous system in vertebrate animals. Several biogenic amines, when excreted, stimulate trace amine-associated receptors (TAARs), a group of GPCRs in the main olfactory epithelium, and elicit innate behaviors. How TAARs recognize amines with varying numbers of amino groups...

The lampricides 3-trifluoromethyl-4-nitrophemol (TFM) and niclosamide have been used for over 60 years to control the invasive sea lamprey (Petromyzon marinus) population in the Laurentian Great Lakes. In this review, we summarize these findings in the context of the mode of action of both lampricides, with a focus on: (1) the physiology of uptake,...

Predator encounters during early life can elicit behavioral and physiological responses that have fitness consequences during subsequent prey life stages. In threatened lake sturgeon (Acipenser fulvescens) and other lithophilic-spawning fishes, newly hatched larvae (free embryos) are exposed to abundant predators including aquatic insect larvae tha...

Pheromonal bile salts are important for sea lampreys ( Petromyzon marinus Linnaeus) to complete their life cycle. The synthesis and release of a releaser/primer pheromone 3-keto petromyzonol sulfate (3kPZS) by spermiating males have been well characterized. 3kPZS evokes sexual behaviors in ovulatory females, induces immediate 3kPZS release in sperm...

The sea lamprey, Petromyzon marinus, is a destructive invader in the Laurentian Great Lakes that relies on several complex chemical cues to complete their life cycle. The central roles of chemical cues in sea lamprey reproduction provide opportunities to leverage knowledge of sea lamprey chemical ecology when developing alternative or supplemental...

Goldfish is an ornamental fish with diverse phenotypes. However, the limited genomic resources of goldfish hamper our understanding of the genetic basis for its phenotypic diversity. To provide enriched genomic resources and infer possible mechanisms underlying skin pigmentation, we performed a large-scale transcriptomic sequencing on 13 adult gold...

Male olfactory cues may guide aggregation on spawning reefs, mate evaluation and synchronized gamete release in lake trout Salvelinus namaycush, but a lack of information on the source and identity of the cues precludes direct tests of their function. Using a two‐channel flume, we found ovulated female lake trout increased time spent in the channel...

Sea lampreys (Petromyzon marinus) are basal vertebrates that exhibit reproductive control via a hypothalamic-pituitary-gonadal axis. The function and evolution of the hypothalamic and pituitary peptide hormones are well studied in this species, whereas the functions of classical sex steroid hormones have not been well established due to their low o...

Chemokine-induced chemotaxis of leukocytes is an important part of the innate immunity and has been shown to mediate inflammation in all groups of jawed vertebrates. For jawless vertebrates, hagfish leukocytes are known to show chemotaxis toward mammalian complement anaphylotoxin and Gram-negative bacteria lipopolysaccharide. However, whether chemo...

Pheromones are chemical signals that elicit innate and stereotyped responses in conspecifics, often with intricate species specificity. The remarkable diversity of pheromones has made them particularly useful for studying the physiological and evolutionary mechanisms underlying communication. However, most discussions on pheromone evolution focus o...

Goldfish (Carassius auratus auratus) are important ornamental fish that have experienced extreme anthropogenic selection and exhibit diverse phenotypes. Loss of the dorsal fin is a key characteristic that distinguishes the Egg-goldfish from the Wen-goldfish. However, the mechanisms underlying the divergence in dorsal fin development are still unkno...

Pheromones play critical roles in habitat identification and reproductive behavior synchronization in the sea lamprey ( Petromyzon marinus ). The bile acid 3-keto petromyzonol sulfate (3kPZS) is a major component of the sex pheromone mixture from male sea lamprey that induces specific olfactory and behavioral responses in conspecific individuals. O...

Sexual signals evolve via selective pressures arising from male-male competition and female choice, including those originating from unintended receivers that detect the signal. For example, males can acquire information from other males signaling to females and alter their own signal. Relative to visual and acoustic signals, less is known about ho...

Significance In many animals, males deceive females into mating using traits that mimic cues of food, predators, preferred habitats, or offspring in need of care. However, if and how these deceptive signals guide reliable communication without females confusing the mimic and the model remain unclear. We discovered that female sea lamprey discrimina...

The American eel (Anguilla rostrata) is an imperilled fish hypothesized to use conspecific cues, in part, to coordinate long‐distance migration during their multistage life history. Here, holding water and tissue from multiple American eel life stages was collected and analysed for the presence, profile and concentration of bile acids. Distinct bil...

Use of the first fish pheromone biopesticide, 3-keto petromyzonol sulfate (3kPZS) in sea lamprey (Petromyzon marinus) control requires an understanding of both how the amount 3kPZS applied to a trap relates to catch, and how that relationship varies among stream types. By conducting 3kPZS dose-response experiments over two years and across six vari...

Quantifying transgenerational effects of stress is important to predict outcomes of anthropogenic disturbances for wildlife species. Maternal stress can programme physiological and behavioural phenotypes in offspring, which may be maladaptive if maternal and offspring environments are mismatched. We investigated effects of a match and mismatch betw...

Biliary atresia (BA) is a rare neonatal disease with unknown causes. Approximately 10% of BA cases develop in utero with other congenital defects that span a large spectrum of disease variations, including degeneration of the gall bladder and bile duct as well as malformation of the liver, intestines, and kidneys. Similar developmental alterations...

Population control of invasive sea lamprey relies heavily on lampricide treatment of infested streams. The lampricide 3-trifluoromethyl-4-nitrophenol (TFM) is thought to impair mitochondrial ATP production through uncoupling oxidative phosphorylation. However, the effect of TFM on the entire electron transport chain (complexes I to V) in the mitoch...

The relationships between pheromone stimuli and neuropeptides are not well established in vertebrates due to the limited number of unequivocally identified pheromone molecules. The sea lamprey (Petromyzon marinus) is an advantageous vertebrate model to study the effects of pheromone exposure on neuropeptides since many pheromone molecules and neuro...

Early life stress can lead to long-term behavioural and physiological phenotypic alterations that impact fitness. Understanding effects of environmental stressors on wildlife is important to predict individual and population-level responses to stressors associated with climate change. Lake sturgeon, Acipenser fulvescens, are a regionally threatened...

Myeloid differentiation factor 88 (MyD88) is a key adaptor of Toll-like receptors (TLR), an important pattern recognition receptor of the innate immune system. To study the origin and evolution of the vertebrate TLR signaling pathway in innate immune systems, we analyzed the biological characteristics and functions of the MyD88 gene in Northeast Ch...

The innate immune response can be activated by infection via different routes. Zebrafish provide a useful infection model for studying inflammation and the innate immune response. We investigated the genes and signaling pathways activated by static immersion and caudal vein microinjection infection using transcriptome profiling and reverse-transcri...

Semen is fundamental for sexual reproduction. The non-sperm part of ejaculated semen, or seminal plasma, facilitates the delivery of sperm to the eggs. The seminal plasma of some species with internal fertilization contains anti-aphrodisiac molecules that deter promiscuity in post-copulatory females, conferring fitness benefits to the ejaculating m...

Background: DDX19 is known as for its role in mRNA transport. It is also involved in translation and innate immune responses. However, the function of Ddx19 during body development rarely reported. We know that ddx19 plays an important role in development of organisms, but we don't understand how it affects the process of cell development. Results:...

Background: Nuclear progesterone receptor (nPR) is an evolutionary innovation in vertebrates that mediates genomic responses to progesterone. Vertebrates also respond to progesterone via membrane progesterone receptors (mPRs) or membrane associated progesterone receptors (MAPRs) through rapid nongenomic mechanisms. Lampreys are extant agnathan ver...

Pheromones are important sexual signals in most animals, but research into their evolution is largely biased toward insects. Lampreys are a jawless fish with a relatively well-understood pheromone communication system, and they offer a useful opportunity to study pheromone evolution in a vertebrate. Once sexually mature, male sea lamprey (Petromyzo...

Giant grouper (Epinephelus lanceolatus) is the largest coral reef teleost, with a native range that spans temperate and tropical‐waters in the Pacific and the Indian Oceans. It is artificially cultured and used as a breeding species in aquaculture due to its rapid growth rate. Here we report a giant grouper genome assembled at the chromosome‐scale...

Three novel bile acid derivatives, petromylidenes A–C (1–3), featuring uncommon alkylidene adductive scaffolds, were isolated from water conditioned with sexually mature male sea lampreys (Petromyzon marinus). Their structures were elucidated by mass spectrometry and NMR spectroscopy, and by comparison to spectral data of related structures. The id...

Significance Anadromous fishes are those that migrate from the ocean into freshwater to reproduce and need to orient toward a suitable spawning stream or risk leaving no offspring. These migrants are known to use olfactory cues to guide stream selection, but the cues’ identities are not known. Incidentally, it is well-known that stream-dwelling lar...

Bioassay-guided fractionation is an iterative approach that uses the results of physiological and behavioral bioassays to guide the isolation and identification of an active pheromone compound. This method has resulted in the successful characterization of the chemical signals that function as pheromones in a wide range of animal species. Sea lampr...

Both enantiomers of petromyroxol are putative pheromones in sea lamprey (Petromyzon marinus). Here, we describe the separation and quantification of the petromyroxol enantiomers using high‐performance liquid chromatography tandem mass spectrometry. The separation was tested on a wide range of chiral columns with normal phases, and effects of the ch...

Covering: up to 2018 Fish use a diverse collection of molecules to communicate with conspecifics. Since Karlson and Lüscher termed these molecules ‘pheromones’, chemists and biologists have joined efforts to characterize their structures and functions. In particular, the understanding of insect pheromones developed at a rapid pace, set, in part, by...

Ligand-based virtual screening has become a standard technique for the efficient discovery of bioactive small molecules. Following assays to determine the activity of compounds selected by virtual screening, or other approaches in which dozens to thousands of molecules have been tested, machine learning techniques make it straightforward to discove...

Zebrafish embryo and larva represent a useful in vivo model for identification of host innate immune responses to bacterial infection. Vibrio parahaemolyticus is a typical zoonotic pathogen worldwide that causes acute gastroenteritis in humans and vibriosis in fishes. However, the mechanism of the innate immune response in the zebrafish larvae infe...

While the advantage of screening vast databases of molecules to cover greater molecular diversity is often mentioned, in reality, only a few studies have been published demonstrating inhibitor discovery by screening more than a million compounds for features that mimic a known three-dimensional (3D) ligand. Two factors contribute: the general diffi...

While the advantage of screening vast databases of molecules to cover greater molecular diversity is often mentioned, in reality, only a few studies have been published demonstrating inhibitor discovery by screening more than a million compounds for features that mimic a known three-dimensional ligand. Two factors contribute: the general difficulty...

CRISPR/Cas9 system has been proven to be an efficient and precise genome editing technology in various organisms. However, the gene editing efficiencies of Cas9 proteins with a nuclear localization signal (NLS) fused to different termini and Cas9 mRNA have not been systematically compared. Here, we compared the ability of Cas9 proteins with NLS fus...

The sea lamprey (Petromyzon marinus) is a destructive invasive species in the Great Lakes that contributed to the collapse of native fish populations in the mid-1900s. 3-Trifluoromethyl-4-nitrophenol (TFM) is a selective pesticide that has been applied to sea lamprey infested tributaries of the Great Lakes to kill larvae since the 1960s and has red...

The sea lamprey (Petromyzon marinus) is a destructive invasive species in the Great Lakes. Since the 1960s, tons of the lampricide 3-trifluoromethyl-4-nitrophenol (TFM) has been applied to selected tributaries each year to eliminate or reduce sea lamprey larval populations. Therefore, the environmental impact of TFM needs to be evaluated. However,...

Vibrio parahaemolyticus (Vp) is an aquatic zoonotic pathogen that causes vibriosis in marine animals as well as sepsis, gastroenteritis and wound infection in human. In vertebrates, the innate immune system plays a critical defense mechanism against Vp infection including transmigration of neutrophils. In this study, we have examined the genetic re...

Deciding where to reproduce is a major challenge for most animals. Many select habitats based upon cues of successful reproduction by conspecifics, such as the presence of offspring from past reproductive events. For example, some fishes select spawning habitat following odors released by juveniles whose rearing habitat overlaps with spawning habit...

Pheromones are among the most important sexual signals used by organisms throughout the animal kingdom. However, few are identified in vertebrates, leaving the evolutionary mechanisms underlying vertebrate pheromones poorly understood. Pre-existing biases in receivers’ perceptual systems shape visual and auditory signaling systems, but studies on h...

Male body size affects access to mates in many animals. Attributes of sexual signals often correlate with body size due to physiological constraints on signal production. Larger males generally produce larger signals, but costs of being large or compensation by small males can result in smaller males producing signals of equal or greater magnitude....

Studies of the voltage-gated sodium (Nav) channels of extant gnathostomes have made it possible to deduce that ancestral gnathostomes possessed four voltage-gated sodium channel genes derived from a single ancestral chordate gene following two rounds of genome duplication early in vertebrates. We investigated the Nav gene family in two species of l...

Two novel sulfated bile salt-like dienones, featuring either a unique, rearranged side chain or a rare cis-11,12-diol on the steroidal C-ring, herein named petromyzene A (1) and B (2), respectively, were isolated from water conditioned with spawning male sea lamprey (Petromyzon marinus; a jawless vertebrate animal). The structures of these natural...

American Eel Anguilla rostrata abundance has declined in recent decades, in part because sexually maturing, silver-stage adults, outmigrating from freshwater to oceanic spawning grounds, encounter migratory blockades or perish when passing through active hydroelectric turbines. To help improve downstream passage effectiveness and increase survival...

Sea lamprey, Petromyzon marinus, rely heavily on chemical cues that mediate their life history events, such as migration and reproduction. Here, we describe petromyzone A-C (1-3), three novel bile alcohols that are highly oxidized and sulfated, isolated from water conditioned with spermiated male sea lamprey. Structures of these compounds were uneq...

Rapid evolution of pest, pathogen, and wildlife populations can have undesirable effects, for example, when insects evolve resistance to pesticides or fishes evolve smaller body size in response to harvest. A destructive invasive species in the Laurentian Great Lakes, the sea lamprey (Petromyzon marinus) has been controlled with the pesticide 3-tri...

This article describes the development and validation of a sensitive LC-MSMS method for determination of estrogen in fish plasma. Dansyl chloride derivatization of the phenol functional group in estrogen was used to enhance the response to atmospheric ionization leading to improve the sensitivity. Individual ¹³C internal standards were selected aft...

Olfactory sensory neurons innervate the olfactory bulb, where responses to different odorants generate a chemotopic map of increased neural activity within different bulbar regions. In this study, insight into the basal pattern of neural organization of the vertebrate olfactory bulb was gained by investigating the lamprey. Retrograde labeling estab...

The pouched lamprey (Geotria australis), one of four Southern Hemisphere lamprey species, is New Zealand’s only freshwater representative of the agnathans. In contrast to that of Northern Hemisphere lampreys, the reproductive ecology of Southern Hemisphere lampreys is poorly understood, with no documented nesting sites or spawning behaviours. In th...

The present study investigated the potential role of conspecific chemical cues in inland juvenile American eel Anguilla rostrata migrations by assessing glass eel and 1 year old elver affinities to elver washings, and elver affinity to adult yellow eel washings. In two-choice maze assays, glass eels were attracted to elver washings, but elvers were...

A UPLC-MS/MS method was developed to provide a reproducible, sensitive and quantitative assay to determine thyroid hormones in sea lamprey tissues and plasma. L-thyroxine (T4) and its two triiodo-thyronine isomers have been simultaneously quantified and validated for plasma, gill, liver, and kidney matrices. Multiple sample preparation techniques w...

Female round gobies were placed in the middle of a four-way maze that received either of these steroids released by reproductive males: 1) 3α-hydroxy-5β-androstane-11,17-dione-3-sulfate (11-O-ETIO-3-S), previously shown to be synthesized by the testes, to be present in the urine of males and to be detected at very low concentrations by the olfactor...

Animals rely on a mosaic of complex information to find and evaluate mates. Pheromones, often comprised of multiple components, are considered to be particularly important for species-recognition in many species. While the evolution of species-specific pheromone blends is well-described in many insects, very few vertebrate pheromones have been stud...

A sensitive and reliable method was developed and validated for the determination of unsaturated bile alcohols in sea lamprey tissues using liquid-liquid extraction and ultra-high performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS). The liver, kidney, and intestine samples were extracted with acetonitrile and defatted by n-hexa...

The American Eel Anguilla rostrata has experienced staggering population declines in recent decades and is now the focus of restoration efforts. Studies have demonstrated that olfaction is critical to anguillid behavior and that glass eels (the life stage which migrates inland from saltwater to freshwater) are attracted to conspecific washings. We...

Control of sea lamprey Petromyzon marinus in the Great Lakes requires accurate assessment of the instream distribution of this pest species and the ability to distinguish it from the four lamprey species that are native to the Great Lakes (American brook lamprey Lethenteron appendix, chestnut lamprey Ichthyomyzon castaneus, northern brook lamprey I...

Analytical methods using liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) for the simultaneous determination of metabolites or contaminants (or both) in various tissues of aquatic organisms and in the aquatic environment have received increasing attention in the last few years. This review discusses the findings relevant to such...

Cholestasis is an impairment of bile formation and bile flow, manifested by secretory defects of hepatocytes or cholangiocytes (or both), or obstruction of bile ducts. Many adaptations occur during cholestasis, including decreases in bile acid synthesis, induction of bile acid detoxification systems, recruitment of alternative export pumps, and inc...

Lampreys are extant representatives of agnathans. Descriptions of lamprey development, physiology and genome have provided critical insights into early evolution of vertebrate traits. However, efficient means for genetic manipulation in agnathan species have not been developed, hindering functional studies of genes in these important Evo-Devo model...

Synchronization of male and female locomotor activity plays a critical role in ensuring reproductive success, especially in semelparous species. The goal of this study was to elucidate the effects of individual chemical signals, or pheromones, on the locomotor activity in the sea lamprey (Petromyzon marinus). In their native habitat, adult preovula...

High resolution mass spectrum report for synthesized DkPES ammonium salt (HR-ESI-MS). (DOCX)

Percentage of sexually mature female sea lamprey that moved upstream 45 m (Up) to side-by-side nest antennas activated with pheromone treatments. (DOCX)

All tracks and plumes for all treatments during field trials. Treatments and ratios are described in Fig 3. (DOCX)

DSC scan and purity analysis for the synthetic DkPES (heating rate = 1.0°C/min, sample weight = 3.20 mg). (DOCX)

All relevant data are within the paper and its Supporting Information files. (XLSX)

Unique mixtures of pheromone components are commonly identified in insects, and have been shown to increase attractiveness towards conspecifics when reconstructed at the natural ratio released by the signaler. In previous field studies of pheromones that attract female sea lamprey (Petromyzon marinus, L.), putative components of the male-released m...

The sensory trap model of signal evolution hypothesizes that signalers adapt to exploit a cue used by the receiver in another context. Although exploitation of receiver biases can result in conflict between the sexes, deceptive signaling systems that are mutually beneficial drive the evolution of stable communication systems. However, female respon...

Background: Biliary atresia (BA) is a human infant disease with inflammatory fibrous obstructions in the bile ducts and is the most common cause for pediatric liver transplantation. In contrast, the sea lamprey undergoes developmental BA with transient cholestasis and fibrosis during metamorphosis, but emerges as a fecund adult. Therefore, sea lam...

Chemical cues and pheromones guide decisions in organisms throughout the animal kingdom. The neurobiology, function, and evolution of olfaction are particularly well described in insects, and resulting concepts have driven novel approaches to pest control. However, aside from several exceptions, the olfactory biology of vertebrates remains poorly u...