Gonochorism vs. hermaphroditism: relationship between life history and fitness in three species of Ophryotrocha (Polychaeta: Dorvilleidae) with different forms of sexuality

1. The relationships between life history, fitness and sexuality, together with their ecological and evolutionary significance, has been analysed comparing the main life-history traits and demography in three closely related species belonging to the genus Ophryotrocha. The species are: the gonochoristic O. labronica, the simultaneous hermaphrodite O. diadema and the protandrous hermaphrodite O. puerilis. 2. Survivorship and reproductive data were collected weekly and were used to construct life tables and population projection matrices for each species and compare life-history characteristics. Elasticity, life-table response and decomposition analyses were performed to examine the relative contribution of fecundity and survivorship to differences in lamda between species. 3. The gonochoristic and hermaphroditic species differ in all the main life-history parameters and also in demographic characteristics. In particular the value of lamda, used commonly to express fitness, is markedly higher in the gonochoristic species while in terms of fitness simultaneous and sequential hermaphroditism are very similar. In the genus Ophryotrocha gonochorism currently represents the most widespread condition, being characteristic of the majority of the known species in the genus. 4. Given the demographic advantage ensured by gonochorism, it remains be understood why some species have retained simultaneous hermaphroditism and one has evolved a sequential type hermaphroditism; the most probable hypothesis is correlated with the density of the species in natural habitats.     

Evolution of the Reproductive Mechanisms in Tardigrades — A Review

Although tardigrades can reproduce only through gametes they have exploited several modes of reproduction, which may be determined by their environment. Marine species (mainly heterotardigrades) are gonochoristic; hermaphroditism is only cited once, and parthenogenesis is unknown. In many cases females mature one egg at a time throughout adult life, whereas males are semelparous. Gonochorism is still present in limno-terrestrial species, while sporadic hermaphroditism occurs in several eutardigrade families. Thelytoky is the most common mode of reproduction in non-marine Tardigrada. Females are iteroparous, laying groups of eggs (free or in the exuvium), while males are semelparous (in a limnic species) or iteroparous with a continuous or cyclical maturation of the spermatozoa (in species from moss and leaf litter). Self-fertilisation appears to characterise hermaphroditic species, found in freshwater, mosses, leaf litter and soil. Egg maturation in these species is similar to that of the gonochoristic species, while spermatozoa mature in appreciable numbers before the oocytes, subsequently maturing continuously but in small numbers over the life of the animal. Parthenogenesis in limno-terrestrial tardigrades always appears continuous. In many species only females occur, but morpho-species populations may be found with both bisexual amphimictic (diploid) and unisexual thelytokous (often but not always polyploid) cytotypes. We can hypothesise that with the evolution of cryptobiosis and passive dispersal unstable and isolated habitats may favour parthenogenesis and self-fertilisation, as both reproductive modes allow colonisation of a new territory by a single individual. Parthenogenesis and hermaphroditism do not occur in the same species, and we can surmise that self-fertilisation will only evolve where parthenogenesis has never occurred.     

Characterization of the sexual pattern of Parastacus varicosus (Crustacea: Decapoda: Parastacidae)

Abstract. Freshwater crayfishes of the genus Parastacus are intersex, i.e., show characteristics of both sexes in the same individual; also, intersexuality has been documented in hermaphroditic species. The aim of this study was to analyze the gonads of Parastacus varicosus , characterizing its sexual pattern. The animals were collected at Cova do Touro, Gravataí, Rio Grande do Sul, Brazil. Three sexual forms were identified: intersex females, intersex males, and transitional specimens showing an ovotestes gonad that could only be identified by means of histological analysis. All specimens had two pairs of gonopores and gonoducts. The oviduct had a wider diameter in females, whereas in males the vasa deferentia were more developed. Gonads were composed of two parallel structures located in the cephalothorax. Female gonads were classified into three stages. The presence of transitional specimens may indicate that sex change occurs, with protandric hermaphroditism, as observed in other species of Parastacus . Because previous studies had demonstrated that P. varicosus is a gonochoristic species in a population from Uruguay, the present study addressed the possibility that the sexual pattern depends on differences in environmental factors among populations. To improve understanding of evolution of hermaphroditism in these crustaceans, their reproductive dynamics should be studied, including identification of the factors stimulating male and female functions.     

Evolutionary transitions among dioecy,androdioecy and hermaphroditism in limnadiid clam shrimp (Branchiopoda: Spinicaudata)

Examinations of breeding system transitions have primarily concentrated on the transition from hermaphroditism to dioecy, likely because of the preponderance of this transition within flowering plants. Fewer studies have considered the reverse transition: dioecy to hermaphroditism. A fruitful approach to studying this latter transition can be sought by studying clades in which transitions between dioecy and hermaphroditism have occurred multiple times. Freshwater crustaceans in the family Limnadiidae comprise dioecious, hermaphroditic and androdioecious (males + hermaphrodites) species, and thus this family represents an excellent model system for the assessment of the evolutionary transitions between these related breeding systems. Herein we report a phylogenetic assessment of breeding system transitions within the family using a total evidence comparative approach. We find that dioecy is the ancestral breeding system for the Limnadiidae and that a minimum of two independent transitions from dioecy to hermaphroditism occurred within this family, leading to (1) a Holarctic, all‐hermaphrodite species, Limnadia lenticularis and (2) mixtures of hermaphrodites and males in the genus Eulimnadia. Both hermaphroditic derivatives are essentially females with only a small amount of energy allocated to male function. Within Eulimnadia, we find several all‐hermaphrodite populations/species that have been independently derived at least twice from androdioecious progenitors within this genus. We discuss two adaptive (based on the notion of ‘reproductive assurance’) and one nonadaptive explanations for the derivation of all‐hermaphroditism from androdioecy. We propose that L. lenticularis likely represents an all‐hermaphrodite species that was derived from an androdioecious ancestor, much like the all‐hermaphrodite populations derived from androdioecy currently observed within the Eulimnadia. Finally, we note that the proposed hypotheses for the dioecy to hermaphroditism transition are unable to explain the derivation of a fully functional, outcrossing hermaphroditic species from a dioecious progenitor.     

A molecular phylogenetic analysis of reproductive trait evolution in the soft coral genus Alcyonium

The soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.     

Evolution of sperm size in nematodes: sperm competition favours larger sperm

In the free-living rhabditid nematode Caenorhabditis elegans, sperm size is a determinant of sperm competitiveness. Larger sperm crawl faster and physically displace smaller sperm to take fertilization priority, but not without a cost: larger sperm are produced at a slower rate. Here, we investigate the evolution of sperm size in the family Rhabditidae by comparing sperm among 19 species, seven of which are hermaphroditic (self-fertile hermaphrodites and males), the rest being gonochoristic (females and males). We found that sperm size differed significantly with reproductive mode: males of gonochoristic species had significantly larger sperm than did males of the hermaphroditic species. Because males compose 50% of the populations of gonochoristic species but are rare in hermaphroditic species, the risk of male-male sperm competition is greater in gonochoristic species. Larger sperm have thus evolved in species with a greater risk of sperm competition. Our results support recent studies contending that sperm size may increase in response to sperm competition.     

Hermaphroditism in fishes: an annotated list of species,phylogeny, and mating system

Fewer than 1% of vertebrate species are hermaphroditic, and essentially all of these are fishes. Four types of hermaphroditism are known in fishes: simultaneous (or synchronous) hermaphroditism (SH), protandry (male-to-female sex change; PA), protogyny (female-to-male sex change; PG), and bidirectional sex change (BS or reversed sex change in protogynous species). Here we present an annotated list of hermaphroditic fish species from a comprehensive review and careful re-examination of all primary literature. We confirmed functional hermaphroditism in more than 450 species in 41 families of 17 teleost orders. PG is the most abundant type (305 species of 20 families), and the others are much less abundant, BS in 66 species of seven families, SH in 55 species of 13 families, and PA in 54 species of 14 families. The recently proposed phylogenetic tree indicated that SH and PA have evolved several times in not-closely related lineages of Teleostei but that PG (and BS) has evolved only in four lineages of Percomorpha. Examination of the relation between hermaphroditism type and mating system in each species mostly supported the size-advantage model that predicts the evolution of sequential hermaphroditism. Finally, intraspecific variations in sexual pattern are discussed in relation to population density, which may cause variation in mating system.

     

Evolution of heteromorphic sex chromosomes in the order Aulopiformes

The fish order Aulopiformes contains both synchronously hermaphroditic and gonochoristic species. From the cytogenetic viewpoint, few reports show that gonochoristic Aulopiformes have heteromorphic sex chromosomes. Because fish in this order give us a unique opportunity to elucidate the evolution of sex chromosomes, it is important to examine a phylogenetic relationship in Aulopiformes by both molecular evolutionary and cytogenetic methods. Thus, we conducted molecular phylogenetic and cytogenetic studies of six Aulopiform species. Our results suggested that hermaphroditic species were evolutionarily derived from gonochoristic species. It follows that the hermaphroditic species might have lost the heteromorphic sex chromosomes during evolution. Here, we suggest a possibility that heteromorphic sex chromosomes can disappear from the genome, even if they have appeared once in evolution. Taking into account Ohno's hypothesis that heteromorphic sex chromosomes might have emerged from autosomes, we propose the hypothesis that heteromorphic sex chromosomes may have undergone repeated events of appearance and disappearance during the course of fish evolution.     

Sexual system in the tanaidacean Falsapseudes bowmani (Crustacea: Malacostraca: Peracarida)

With more than 40,000 species, Malacostraca is the most diverse crustacean class. Most malacostracans are gonochoristic, but simultaneous hermaphrodites are also known. Tanaidacea is one of two malacostracan orders that includes simultaneously hermaphroditic species; so far, simultaneous hermaphroditism has been confirmed externally and internally in only two tanaidacean species, both in the genus Apseudes (Apseudidae). Here we show, through external and internal morphological observations of fixed specimens, that the apseudid Falsapseudes bowmani is a simultaneous hermaphrodite, making Falsapseudes the second tanaidacean genus in which simultaneous hermaphroditism has been confirmed both externally and internally. In this species, the epistome (a projection on the clypeus) was thick and elongate in large specimens but was thin and spiniform in smaller specimens; the brooding of eggs or embryos was observed only in thin‐epistome individuals, although a pair of ovaries was confirmed in both thick‐ and thin‐epistome individuals. This suggests that individuals with a thick epistome may act as males while also retaining the female reproductive organs.     

Sexual determination and differentiation in teleost fish

The present work reviews the latest information on the cellular, molecular and physiological aspects of sexual determination and differentiation in teleost fish. The group exhibits a large variety of mechanisms of sexual determination. These may be genetic, or depend on environmental conditions such as temperature, pH, and social factors, all of which can influence the proportion of the sexes. Additionally, sex steroids play an important role in the regulation of sexual differentiation. The patterns of gonadal sexual differentiation are diverse, and species may be hermaphroditic or gonochoristic, some of the latter displaying juvenile hermaphroditism. In recent years, several genes involved in the sexual determination and differentiation pathways in vertebrates, particularly in mammals, have also been characterized in teleosts. Conserved as well as diversified functions have been proposed.     

Sexual reproduction of Hawaiian black corals,with a review of the reproduction of antipatharians (Cnidaria: Anthozoa: Hexacorallia)

Abstract. Black corals (Cnidaria: Antipatharia) are ecologically important members of the sessile invertebrate fauna, but due to their typical deep‐water environments (>50 m), very little is known about their basic biology, including reproduction. We used histological techniques to examine the sexual reproduction of members of eight species of antipatharians collected from the Hawaiian Islands over a wide depth range (10–1327 m). Gametes of all species examined were found in association with the primary transverse mesenteries, which in some cases reached into the cavity of lateral tentacles. Specimens contained either spermatocysts or oocytes, but never both within the same individual, suggesting either a gonochoric or a sequentially hermaphroditic mode of reproduction. No developing embryos or larvae were observed in any of the samples, indicating that fertilization and larval development likely occur externally in the water column and not internally within polyps. We compared our results with previously published information on the sexual reproduction of antipatharians. Our review suggests that in antipatharians, more generally, (1) entire colonies are either female or male (although sequential hermaphroditism cannot be ruled out in most cases and has been reported previously for one species), (2) gametes are confined to the primary transverse mesenteries in most species, and (3) there is no evidence of internal fertilization. Further studies are needed to determine whether gonochorism or sequential hermaphroditism is more prevalent within the Antipatharia, whether dimorphic polyps occur within this taxonomic order, and to examine the reproductive seasonality and larval behavior of individual species.     

Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals

Excluding insects, hermaphroditism occurs in about one-third of animal species, providing numerous opportunities for the evolution of selfing. Here we provide an overview of reproductive traits in hermaphroditic animal species, review the distribution of selfing rates in animals, and test for ecological correlates of selfing. Our dataset (1342 selfing-rate estimates for 142 species) is 97% based on estimates derived from the analysis of population structure (F(IS)-estimates) using genetic markers. The distribution of selfing is slightly U-shaped and differs significantly from the more strongly U-shaped plant distribution with 47% of animal t-estimates being intermediate (falling between 0.2 and 0.8) compared to 42% for plants. The influence of several factors on the distribution of selfing rates was explored (e.g., number of populations studied per species, habitat, coloniality, sessility, or fertilization type), none of which significantly affect the distribution. Our results suggest that genetic forces might contribute to the evolution of self-fertilization to the same extent in animals and plants, although the high proportion of intermediate outcrossing suggests a significant role of ecological factors (e.g., reproductive assurance) in animals. However, we caution that the distribution of selfing rates in animals is affected by various factors that might bias F(IS)-estimates, including phylogenetic underrepresentation of highly selfing and outcrossing species, various genotyping errors (e.g., null alleles) and inbreeding depression. This highlights the necessity of obtaining better estimates of selfing for hermaphroditic animals, such as genotyping progeny arrays, as in plants.     

Extremely high molecular diversity within the East Asian nematode Caenorhabditis sp. 5

Most relatives of the self-fertilizing hermaphroditic nematode model organism Caenorhabditis elegans reproduce via obligate outbreeding between males and females, which also represents the ancestral mode of reproduction within the genus. However, little is known about the scope of genetic diversity and differentiation within such gonochoristic species, especially those found outside of temperate Europe and North America. It is critical to understand the evolutionary processes operating in these species to provide a framework for deciphering the evolution of hermaphroditism and a baseline for the application of outcrossing Caenorhabditis to problems in evolutionary genetics. Here, we investigate for the first time molecular sequence variation for Caenorhabditis sp. 5, a species found commonly in eastern Asia. We identify enormous levels of standing genetic variation that approach the levels observed in the marine broadcast-spawning sea squirt, Ciona savignyi. Although we document significant isolation by distance, we demonstrate that the high polymorphism within C. sp. 5 is not because of strong differentiation among populations or to the presence of cryptic species. These findings illustrate that molecular population genetic approaches to studying obligately outbreeding species of Caenorhabditis will prove powerful in identifying and characterizing functionally and evolutionarily important features of the genome.     

Patterns of gonad structure in hermaphroditic gobies (Teleostei Gobiidae)

Synopsis Hermaphroditism has been reported for a small number of gobiid fishes, but the extent of this sexual pattern within the family is not known. Gonad structure was examined in one or more species from twenty-one gobiid genera. No evidence of hermaphroditism was found in the species selected from 14 genera. Laboratory studies supported the conclusion of gonochorism for the examined species in four of them:Asterropteryx, Bathygobius, Gnatholepis, andPsilogobius. Currently, the absence of precursive testicular tissues associated with the ovary in females, in conjunction with no retained ovarian features in the testes of males, appear to be reliable indicators of a gonochoristic sexual pattern in gobiid fishes. Evidence for hermaphroditism was observed in seven genera:Eviota, Trimma, Fusigobius, Lophogobius, Priolepis, Gobiodon, andParagobiodon. Protogyny was experimentally confirmed inE. epiphanes, and the gonad structure in another nine of ten species ofEviota suggested either protogyny or protogynous tendencies. With the exception ofGobiodon andParagobiodon, which exhibited similar gonadal structure, ovarian and testicular structure varied considerably among the hermaphroditic genera examined, both with regard to the configuration and to the degree of development of ovarian and testicular tissues, or testicular tissue precursors. Findings of this study indicate that hermaphroditic gonad structure will prove to be a useful trait in determining evolutionary relationships within the Gobiidae.     

Sexual development and sexuality in the Nassau grouper

Hermaphroditic sexual patterns are widespread among teleosts and are especially characteristic of certain perciform families. Among the most diverse groups of hermaphroditic species are the groupers, hamlets and sea basses of the family Serranidae. Like other groupers, the epinepheline serranid, Epinephelus striatus , the Nassau grouper, has long been assumed to exhibit monandric protogyny (a form of hermaphroditism in which all males derive from adult females by sex change). Histological and demographic data, however, indicate that the sexual pattern of this species is not monandric, and that, unlike other group species, the juveniles pass through a bisexual stage of gonadal development. Sexuality in the Nassau grouper is essentially gonochoristic, with potential for sex change. The combination of bisexuality and gonochorism is previously undescribed in the serranids.     

THE ROLE OF ANDRODIOECY AND GYNODIOECY IN MEDIATING EVOLUTIONARY TRANSITIONS BETWEEN DIOECY AND HERMAPHRODITISM IN THE ANIMALIA

Dioecy (gonochorism) is dominant within the Animalia, although a recent review suggests hermaphroditism is also common. Evolutionary transitions from dioecy to hermaphroditism (or vice versa) have occurred frequently in animals, but few studies suggest the advantage of such transitions. In particular, few studies assess how hermaphroditism evolves from dioecy or whether androdioecy or gynodioecy should be an “intermediate” stage, as noted in plants. Herein, these transitions are assessed by documenting the numbers of androdioecious and gynodioecious animals and inferring their ancestral reproductive mode. Both systems are rare, but androdioecy was an order of magnitude more common than gynodioecy. Transitions from dioecious ancestors were commonly to androdioecy rather than gynodioecy. Hermaphrodites evolving from sexually dimorphic dioecious ancestors appear to be constrained to those with female‐biased sex allocation; such hermaphrodites replace females to coexist with males. Hermaphrodites evolving from sexually monomorphic dioecious ancestors were not similarly constrained. Species transitioning from hermaphroditic ancestors were more commonly androdioecious than gynodioecious, contrasting with similar transitions in plants. In animals, such transitions were associated with size specialization between the sexes, whereas in plants these transitions were to avoid inbreeding depression. Further research should frame these reproductive transitions in a theoretical context, similar to botanical studies.     

Going solo: discovery of the first parthenogenetic gordiid (Nematomorpha: Gordiida)

Despite the severe fitness costs associated with sexual reproduction, its persistence and pervasiveness among multicellular organisms testifies to its intrinsic, short-term advantages. However, the reproductive assurance hypothesis predicts selection favoring asexual reproduction in sparse populations and when mate finding is difficult. Difficulties in finding mates is especially common in parasites, whose life cycles involve multiple hosts, or being released from the host into the external environment where the parasite can find itself trapped without a sexual partner. To solve this problem and guarantee reproduction, parasites in numerous phyla have evolved reproductive strategies, as predicted by the reproductive assurance hypothesis, such as hermaphroditism or parthenogenesis. However, this type of strategy has not been reported from species in the phylum Nematomorpha, whose populations have often been described as sparse. A new Nematomorpha species, Paragordius obamai n. sp., was discovered from Kenya, Africa, and appears to have solved the problem of being trapped without a mate by eliminating the need for males. Paragordius obamai n. sp. represents the first and only known species within this phylum to reproduce asexually. To determine the mechanism of this mating strategy, we ruled out the involvement of reproduction manipulating endosymbionts by use of next generation sequencing data, thus suggesting that parthenogenesis is determined genetically and may have evolved as a means to assure reproduction. Since this new parthenogenetic species and a closely related gonochoristic North American congener, P. varius, are easy to propagate in the laboratory, these gordiids can be used as model systems to test hypotheses on the genetic advantages and disadvantages of asexual reproduction and the genetic determinants of reproductive strategies in parasites.     

Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA

DNA sequences of the second internal transcribed spacer (ITS2) of ribosomal DNA (rDNA) were determined for 11 species from four genera of Didymozoinae (Indodidymozoon, Helicodidymozoon, Rhopalotrema and Neometadidymozoon) and a species of the Lecithasteridae, Lecithaster stellatus. Sequences were used to test the validity of species recognised on morphological criteria and to infer phylogenetic relationships. Sequences of the 11 didymozoids differed by 0.5% to 19%. Our phylogenetic analyses: (i) indicate that species in the genera Helicodidymozoon and Rhopalotrema are a monophyletic group; (ii) support separation of the genus Helicodidymozoon from the genera Indodidymozoon and Neometadidymozoon; and (iii) support recognition of Rhopalotrema as a genus distinct from Neometadidymozoon. We found the gonochoristic species, I. pearsoni and I. suttiei, to be genetically similar to the hermaphroditic species in the genus Indodidymozoon and found no evidence to indicate that they belong in a separate genus.     

An analysis of species boundaries and biogeographic patterns in a cryptic species complex: the rotifer--Brachionus plicatilis

Since the advent of molecular phylogenetics, there is increasing evidence that many small aquatic and marine invertebrates--once believed to be single, cosmopolitan species--are in fact cryptic species complexes. Although the application of the biological species concept is central to the identification of species boundaries in these cryptic complexes, tests of reproductive isolation do not frequently accompany phylogenetic studies. Because different species concepts generally identify different boundaries in cryptic complexes, studies that apply multiple species concepts are needed to gain a more detailed understanding of patterns of diversification in these taxa. Here we explore different methods of empirically delimiting species boundaries in the salt water rotifer Brachionus plicatilis by comparing reproductive data (i.e., the traditional biological species concept) to phylogenetic data (the genealogical species concept). Based on a high degree of molecular sequence divergence and largely concordant genetic patterns in COI and ITS1, the genealogical species hypothesis indicates the existence of at least 14 species--the highest estimate for the group thus far. A test of the genealogical species concept with biological crosses shows a fairly high level of concordance, depending on the degree of reproductive success used to draw boundaries. The convergence of species concepts in this group suggests that many of the species within the group may be old. Although the diversity of the group is higher than previously understood, geographic distributions remain broad. Efficient passive dispersal has resulted in global distributions for many species with some evidence of isolation by distance over large geographic scales. These patterns concur with expectations that micro-meiofauna (0.1-1mm) have biogeographies intermediate to microbial organisms and large vertebrates. Sympatry of genetically distant strains is common.     

Molecular evolution in Panagrolaimus nematodes: origins of parthenogenesis, hermaphroditism and the Antarctic species P. davidi

Background  

As exemplified by the famously successful model organism Caenorhabditis elegans, nematodes offer outstanding animal systems for investigating diverse biological phenomena due to their small genome sizes, short generation times and ease of laboratory maintenance. Nematodes in the genus Panagrolaimus have served in comparative development and anhydrobiosis studies, and the Antarctic species P. davidi offers a powerful paradigm for understanding the biological mechanisms of extreme cold tolerance. Panagrolaimus nematodes are also unique in that examples of gonochoristic, hermaphroditic and parthenogenetic reproductive modes have been reported for members of this genus. The evolutionary origins of these varying reproductive modes and the Antarctic species P. davidi, however, remain enigmatic.