First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction

Parthenogenesis, the development of unfertilized eggs resulting in the exclusive production of female offspring, is rare in animals relative to sexual reproduction and is mainly reported in invertebrates. It has been hypothesized that polyploidy, hybridization and endosymbiont infections are its major causal events but the mechanisms triggering asexual reproduction remain unclear. Here, we study the proximate causes at the origin of parthenogenesis in the first reported case of asexuality in the Coccinellidae (Coleoptera). The asexual populations were found in the Azores and the Mascarene archipelagos, and were identified as Nephus voeltzkowi Weise, a bisexual species widespread in sub-Saharan Africa. The specimens from both populations are diploid but present different karyotypes and heterozygosities that evoke hybrid origins, commonly associated with parthenogenesis in Coleoptera. However, the close proximity of their genomes (99.8% homology for the complete mitochondrial genome and 99.9% for the complete nuclear ribosomal cluster) together with the congruence between the mtDNA tree and the nuclear tree, and the low heterozygosity levels, suggests that the two populations are not hybrid. We propose that they belong to a single chromosomally polymorphic species undergoing Robertsonian fusions. Furthermore, specimens from both populations are infected with Wolbachia (supergroup B strain), contrary to sympatric bisexual species of the same genus. Although Wolbachia has been shown to induce parthenogenesis in haplodiploid organisms, it has been recently suggested that it could also induce parthenogenesis in hosts with other sex determination systems. Whether chromosome rearrangements and/or Wolbachia infections are post-parthenogenetic events or are at the origin of parthenogenesis still needs to be determined.     

Home ranges of parthenogenetic and bisexual species in a community of Darevskia lizards (Reptilia: Lacertidae)

We analysed the home ranges of a community of Darevskia rock lizards composed of a bisexual species (D. valentini), two parthenogens (D. armeniaca and D. unisexualis), and two backcross forms between bisexual and unisexual forms. We estimated home range areas of ink-marked, GPS-located lizards using Minimum Convex Polygon (MCP) and 95% of the locations for those individuals with five or more sightings. The bisexual D. valentini was the species with the largest home ranges, distances travelled, and the most intersections. No differences between unisexual species and backcrosses were recorded for any comparison. In males, home range size and perimeter were related to morphological characteristics. Contrary to what has been described in allopatry, unisexual species showed smaller home ranges and fewer overlaps than sympatric bisexual species. We tentatively suggest that the presence of potential bisexual partners might increase sexual competition among parthenogenetic females while differences in habitat use should also be considered.     

Parthenogenesis in Psocids (Insecta: Psocoptera)

SYNOPSIS. Obligate thelytokous parthenogenesis and, more rarely,facultative thelytoky are known to occur in psocids. The formerphenomenon is known in 28 species. The latter is known onlyin two species, both of which have obligatorily thelytokousforms as well as bisexual ones. Attempts to force thelytokousfemales to mate have been carried out for four nominal species.All have failed. Differences in color or color pattern betweenthe bisexual and thelytokous forms of a nominal species havebeen observed in two instances. In Echmepteryx hageni this seemsto involve divergence where the two forms occur sympatricallybut on different habitats. Investigations of geographic distributionof bisexual and thelytokous forms of a nominal species showin several cases that the thelytokous forms are much more widespreadthan the bisexual ones. In eastern United States, bisexual formstend to occur peripherally and in ecologically unusual areas.The areas of occurrence of bisexual populations may be relictual,and some of them may have been Pleistocene refugia. Most ofthese areas correspond to areas where coniferous trees now forman important part of the forest.     

Species recognition by male swordtails via chemical cues

Species recognition can often play a key role in female matingpreferences. Far less is known about conspecific mate recognitionfrom the male perspective. In many closely related taxa, femalesexhibit few obvious visual differences and males might haveto attend to chemical cues in mate recognition, a possibilitythat has rarely been explored in vertebrates. Here, we examinemale species recognition via odor cues in the swordtail fish,Xiphophorus birchmanni. In dichotomous choice experiments wefirst tested whether males respond to female odor cues. We foundthat males were attracted to conspecific female odor and thoseof a related allopatric congener, Xiphophorus malinche, overa water control. Males did not, however, respond to the femaleodor of the more distantly related sympatric platyfish, Xiphophorusvariatus. We then gave male X. birchmanni the choice betweenconspecific and heterospecific female stimuli. Males, in thisscenario, significantly preferred the conspecific odor whenthe alternative was platyfish. However, when offered odor cuesof X. malinche, male X. birchmanni actually preferred the heterospecificfemale cue. The complex array of preferences reported here,previously documented only in females, underscores the needto consider the behavior of both sexes in dictating actual matingoutcomes.     

Genetically identical copies of the mulberry silkworm

Summary Genetically identical copies of the silkworm female obtained via ameiotic parthenogenesis are insignificantly depressed by artificial reproduction, and notwithstanding their isogenous pattern, they show the same variability in quantitative characters as in the heterogenous forms.By means of androgenesis, genetically identical copies of strictly homozygous males were obtained; the latter were produced via meiotic parthenogenesis. The androgenetic clones of these males were transformed by backcrosses into homozygous bisexual lines. Viability and cocoon weight in these lines were higher than those in androgenetic clones of similar genotype, but they were far from the norm due to the depressing effect of semilethals left in them in a homozygous state. An extremely low phenotypical variability of quantitative characters is observed in the isogenous hybrids F₁ obtained from crossing two genetically dissimilar strictly homozygous individuals. These hybrids make excellent material for phenogenetical studies. The female and male isogenous clones have an increased combining ability which is acquired in the course of their selection for high disposition towards complete parthenogenesis. For practical purposes it is proposed to take a female and a male which when mated produce a high-quality family and clone them separately, the first via parthenogenesis, the latter via androgenesis. After mating these reproduced bisexual clones, it will be possible to obtain in successive generations a vast number of families repeating the prominent productivity of the initial family.     

Molecular genetic evidence for parthenogenesis in the Burmese python,Python molurus bivittatus

Parthenogenesis among reptiles is rare. Only a few species have the ability to reproduce asexually. Most of these are obligate parthenogenetic species that consist (almost) entirely of females, which can reproduce solely through parthenogenesis. Rarer are sexual species that only sporadically reproduce through parthenogenesis. A female Python molurus bivittatus (Reptilia, Boidae) from the Artis Zoo, Amsterdam, produced eggs in five consecutive years that contained embryos while she was isolated from males. These eggs might be fertilized with stored sperm, or might be the product of parthenogenesis. Parthenogenesis has not been shown for the Boidae family before. We performed parentship analyses on the snake and seven of her embryos using microsatellites and AFLP. Four microsatellite loci developed for this species combined with three loci developed previously for different snake species revealed too little variation to discriminate between sperm retention and parthenogenesis. With AFLP we were able to confirm that the Artis Zoo female reproduced parthenogenetically. Because the offspring are genetically identical to their mother, whereas in previous studies on sporadic parthenogenesis in snakes a loss of genetic information was reported, we conclude that the meiotic pathways that produce the diploid egg cells are different.     

Evolutionary approaches for studying functional morphology: examples from studies of performance capacity

Performance studies have long been a cornerstone of evolutionarystudies of adaptation because of their purported importancefor fitness. Nevertheless, for most systems, the mechanisticlink among habitat use, morphology and performance is poorlyunderstood. Further, few studies consider how behavior affectsthe relationship between morphology and performance. Here, Ihighlight the utility of considering both of these neglectedareas by discussing studies in two systems: (1) the evolutionof habitat use in Caribbean Anolis lizards, and (2) the evolutionof limb function in desert lizards. Caribbean Anolis lizardspartition the habitat via selection of different perch diameters,and surface diameter also exerts a strong effect on locomotorperformance. Phylogenetic analyses show that Anolis speciestend to avoid using perches in which their performance is submaximal,and also show that species with large performance breadths usea greater range of habitats. The underlying basis of this performanceto habitat use link is a trade-off between the ability to sprintquickly on broad surfaces and the ability to move effectivelyon narrow surfaces. Studies of the kinematics of high-speedlocomotion in five morphologically distinct lizard species revealthat some species exhibited behaviors that greatly enhancedtheir performance abilities relative to other species, suggestingthat behavior can play a key role in the link between morphologyand performance. Overall, these findings underscore the valueof using a mechanistic approach for studying the links betweenhabitat use, morphology and behavior.     

Introgression in the genus Salmo via allotriploids

Hybridization between sympatric species is not uncommon in the wild. Wild allotriploids (individuals with two chromosome sets from a species + one chromosome set from another species) are generally the result of a backcross between interspecific hybrids that produce unreduced gametes and one of the parental species. In animals, allotriploids are commonly sterile, except for some vertebrate species complexes in which allotriploids reproduce by parthenogenesis, gynogenesis and/or hybridogenesis, producing generally clonal or hemiclonal gametes; nuclear DNA introgression between hybridizing species is considered to be extremely rare. Employing species-specific molecular markers, we show genetic introgression between the chromosomally well-differentiated salmonids Atlantic salmon (2n = 58) and brown trout (2n = 80) through spontaneous bisexual reproduction of allotriploids leading to salmon-like offspring bearing some brown trout genes. Although introgression between these Salmo species can occur via allotriploids, we hypothesize that extinction of parental species can be discarded based on very low survival of allotriploid offspring.     

Paternal Care in Canids

Paternal care has never been reported as absent in any canidspecies, and some form of care has been seen in 18 of the 36species in the family. Food provisioning, active defense ofthe young, and protecting young by remaining at the den as thefemale forages appear to be the commonest forms of male care.In addition males may groom, retrieve, play and rest with young.Male canids are rarely involved in den selection or construction.The effect on the fitness of the young of indirect forms ofmale care such as provisioning the female and territory defenseare hard to assess. Quantitative studies of male provisioningin seven species offer few generalizations. In two species (Canisaureus, C mesomelas) females provided more food to the youngthan males; in one species (Alopex lagopus) the pair contributedequally to feeding young, and in four species (Canis lupus,Vulpes vulpes, Chrysocyon brachyurus, and Lycaon pictus), malesprovided more food than females. Much more data are required,particularly from field studies, before patterns of variationcan be interpreted.     

A Review of Size at Maturity in Male Tanner (Chionoecetes bairdi) and King (Paralithodes camtschaticus) Crabs and the Methods Used to Determine Maturity

This paper reviews existing studies on the size of sexual maturityfor male Tanner or snow crab (Chionoecetes bairdi), a brachyuran,and the anomuran red king crab (Paralithodes camtschaticus).In this report the term sexual maturity is denned as the abilityto reproduce. A variety of indirect and direct methods thathave been used to determine maturity are reviewed. Examiningthe vas deferens for the presence of spermatophores was usefulin determining the size at which males first become mature.Breeding experiments in the laboratory demonstrated that mostmales, from both species, that produced spermatophores couldbreed with soft-shelled mates. Males of both species can breedat smaller sizes than do females. Morphometric techniques basedon reproductive tract weights and chela morphometry overestimatedthe sizes at which males mature in both species. Previous experimentsfor Tanner crab, which have internal fertilization, suggestsmall mature males can fertilize two to five females. Breedingexperiments showed recently matured red king crab do not appearto be able to fertilize more than one female per breeding season,while males nearing harvestable size can fertilize more thanone female. Breeding experiments and in situ observations of grasping pairsappear to be the most feasible methods for identifying malesize at maturity for these species. The value of morphometricestimations for determining when males mature is questionable.     

Genetic Polymorphism and Evolution in Parthenogenetic Animals. II. Diploid and Polyploid SOLENOBIA TRIQUETRELLA (Lepidoptera: Psychidae)

Genic polymorphism at sixteen enzyme loci of four different chromosomal races of Solenobia triquetrella (bisexual, two diploid parthenogenetic races and tetraploid parthenogenetic) has been studied by starch gel electrophoresis. Isolated small diploid bisexual populations have rather uniform allele frequencies at all loci which we have studied. Diploid and tetraploid parthenogenetic individuals of this species are in general as heterozygous as bisexual ones. All parthenogenetic local populations are different from each other in the Alps. These parthenogenetic genotypes cannot be derived from a common ancestor through single mutations but rather bear evidence for a polyphyletic origin of parthenogenesis in Solenobia triquetrella. In the marginal distribution areas of the species in northern Europe single genotypes are spread over far larger areas than in the mountain regions of central Europe. This may be due to the old origin of parthenogenesis and polyploidy in northern Europe. No new parthenogenetic and polyploid strains have lately arisen in the regions outside of the Alps.     

Appearance of males in a thelytokous strain of Milnesium cf. tardigradum (Tardigrada)

Tardigrades are generally gonochoristic. Many moss-dwelling species propagate by parthenogenesis, but heterogony has not yet been found. Milnesium tardigradum, a carnivorous tardigrade, also has both sexes, but males are usually rare and many populations appear to have only parthenogenetic reproduction. Since 2000, I have maintained a thelytokous strain of Milnesium cf. tardigradum that originated from one female. Individuals of this strain were thought to be all females, but here I report that males have emerged in this strain at a very low frequency. This is the first report of the appearance of males in parthenogenetic tardigrades. On the first pair of legs of some individuals, I observed the modified claws characteristic of males of this species. It is unknown whether these males can actually function in sexual reproduction; however, they might allow some possibility of genetic exchange among clonal populations. No environmental factors that generate males were determined.     

Preadaptation for parthenogenetic colony foundation in subterranean termites Reticulitermes spp. (Isoptera: Rhinotermitidae)

Thelytokous (all-female producing) parthenogenesis, in some cases, involves reproductive advantages against obligate sexual reproduction. However, the completion of parthenogenesis takes multiple steps without the help of males, and thus preadaptation that meets those requirements will be an important factor for the evolution of parthenogenesis. The Japanese subterranean termite, Reticulitermes speratus, is known to have the ability of parthenogenetic colony foundation, where females that failed to mate with males found colonies cooperatively with partner females and reproduce by parthenogenesis. In this study, we compared the parthenogenetic ability and the colony initiation behavior among six Reticulitermes species in Japan. All species other than R. speratus were not able to reproduce parthenogenetically. Nevertheless, females of these species without the parthenogenetic ability performed homosexual female–female colony initiation and produced eggs without fertilization. In addition, in one species without parthenogenetic reproduction, R. kanmonensis, female–female pair initiated founding behavior as quickly as a heterosexual pair. These results suggest that female–female colony initiation and virgin egg-laying are predominant characters among the genus Reticulitermes and provide a preadaptive condition for parthenogenetic colony foundation in R. speratus.     

Color patterns and species recognition in four closely related species of Lake Malawi cichlid

We examined interspecific female mating preferences in fourclosely related species of cichlid belonging to the Pseudotropheuszebra species complex of Lake Malawi. These species differin coloration but are similar in other respects, suggestingthat male color patterns may be important to female mate choicein species recognition. To test this hypothesis, we presented females from each species with a choice of four males, one ofher own species and three others that were each of a differentspecies. We also gave each female a choice between the threeheterospecific males only. In all four species, females showeda significant preference for conspecific males in the four-waychoice and chose the male with the most similar color patternto the conspecific male in the three-way choice. These resultsare discussed with reference to the theory of sexual selectionon color patterns as a means of sympatric speciation in cichlids.     

Variation in the life cycle of monogonont rotifers: Commitment to sex and emergence from diapause

1. A review of research on life-cycle events in field and laboratory populations of monogonont rotifers shows that there is great variation at multiple levels: (1) degree of sexual dimorphism; (2) occurrence and timing of sex; (3) propensity for sex during sexual periods; (4) factors controlling initiation of sex; and (5) timing and extent of emergence from diapause. There is no regular pattern where: (1) fertilised resting eggs hatch to start the growing season; (2) populations develop via female parthenogenesis during favourable conditions; and then (3) bisexual reproduction with resting-egg production occurs during later, unfavourable conditions.
2. Sexual reproduction in natural populations can occur throughout much of the growing season, be restricted to some period(s) during the growing season, or be completely absent. During sexual reproduction in both natural and laboratory populations, only some fraction of females produces males or resting eggs. This bet-hedging strategy can prevent a population crash and permits future population growth via female parthenogenesis. Selection against sexual reproduction, and rapid loss of sex, can occur.
3. Laboratory experiments with pond-dwelling species have identified specific environmental factors that induce sex in different species: (1) increasing population density; (2) dietary tocopherol (vitamin E) and (3) long photoperiods. These factors generally are associated with favourable conditions for population growth and production of energy-rich resting eggs: (1) large population size; (2) high probability of contacts between males and fertilisable females; and (3) nutritious diets. Endogenous factors can inhibit responses to these environmental inducers, and thus favour female parthenogenesis.
4. The timing of resting-egg hatching depends on: (1) occurrence of specific environmental conditions; (2) the minimum duration of obligate diapause; and (3) the genotype and physiology of females producing resting eggs. Hatching may occur shortly after oviposition, after a long diapause before or at the start of a new growing season, or throughout the growing season. Hatching can be massive and contribute substantially to population growth and genetic diversity.
5. Areas for future research include: (1) determining the timing and extent of sex and resting-egg hatching in more natural populations, especially those that are marine, benthic, sessile, and interstitial; and (2) identifying environmental and physiological factors controlling these events.

     

Relations between microhabitat use and limb shape in phrynosomatid lizards

With the exception of the well-documented case for anoline lizards, recent studies have found few evolutionary relationships between morphology and habitat use in lizards despite clear-cut biomechanical predictions. One of the factors typically hampering these analyses is the clustering of habitat use within evolutionary lineages. In the present study, body shape was quantified for male and female lizards of 30 species of phrynosomatid lizards. This group was selected as little clustering of ecological variables seemed to be present. The results of traditional analyses indicate that evolutionary correlates of habitat use were prominent in the hindlimbs of both sexes. Species living in open habitats are characterized by longer femurs, and longer hindlimbs relative to the forelimb. Moreover, males from ground-dwelling species utilizing open habitats have longer toes on the hind foot than males from climbing species. Phylogenetic analyses indicated strong evolutionary associations between habitat use and the relative length of front and hindlimbs, with species from open terrestrial habitats having significantly shorter frontlimbs relative to their hindlimb than rock or tree climbing species. Evolutionary associations between morphology and habitat use were generally stronger for male lizards, indicating a potentially important contribution of sexual selection to the evolution of differences in limb proportions.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 149–163.     

Comparative paternal and infanticidal behavior of sympatric white-footed mice (Peromyscus leucopus noveboracensis) and deermice (P. maniculatus nubiterrae)

We studied parental and infanticidal behavior in the field andlaboratory in two ecologically equivalent and sympatric congeners,white-footed mice, Peromyscus leucopus noveboracensis, and deermice,P. maniculatus nubiterrae. Despite their close phylogeneticrelationship and ecological similarity, various aspects of parentaland nesting behavior of the two species were significantly different.P. maniculatus males were more paternal than were P. leucopusmales in that they retrieved pups, nested with pregnant femalesand females with newborn pups, and formed longer associationswith females than did P. leucopus males. Thus, P. m. nubiterraeexhibited more pair-bonding (monogamous) characteristics thandid either P. leucopus or P. m. bairdi, as reported in otherstudies. The behavioral differences may represent the differentevolutionary history of the three subspecies. Infanticidal behavior,however, was similar in both species. Dispersing and unmatedmales killed strange pups placed in experimental test chambersin the field, whereas mated males did not kill pups within theirown home ranges. Resident females of both species were moreinfanticidal than were males, killing pups in 90% of the trials.The results support the sexual selection and resource competitionhypotheses for male and female infanticide, respectively. [BehavEcol 1991; 2: 38-45]     

The emerging phylogenetic pattern of parthenogenesis in snakes

Parthenogenesis occurs across a variety of vertebrate taxa. Within squamate reptiles (lizards and snakes), a group for which the largest number of cases has been documented, both obligate and facultative types of parthenogenesis exists, although the obligate form in snakes appears to be restricted to a single basal species of blind snake, Indotyphlops braminus. By contrast, a number of snake species that otherwise reproduce sexually have been found capable of facultative parthenogenesis. Because the original documentation of this phenomenon was restricted to subjects held in captivity and isolated from males, facultative parthenogenesis was attributed as a captive syndrome. However, its recent discovery in nature shifts the paradigm and identifies this form of reproduction as a potentially important feature of vertebrate evolution. In light of the growing number of documented cases of parthenogenesis, it is now possible to review the phylogenetic distribution in snakes and thus identify subtle variations and commonalities that may exist through the characterization of its emerging properties. Based on our findings, we propose partitioning facultative parthenogenesis in snakes into two categories, type A and type B, based on the sex of the progeny produced, their viability, sex chromosome morphology, and ploidy, as well as their phylogenetic position. Furthermore, we introduce a hypothesis (directionality of heterogamety hypothesis) to explain the production of female‐only parthenogens in basal alethinophidian snakes and male‐only parthenogens in caenophidian (advanced) snakes.     

On the Ecology of Coexistence in Parthenogenetic and Bisexual Lizards of the Genus Cnemidophorus

In the center of their distribution in North America, membersof a complex of parthenogenetic and bisexual lizards of thegenus Cnemidophorus may be found side by side with one or moreof the others in a bewildering variety of patterns and ecologicalassociations. Exactly why so many congeneric species are foundliving together and exactly what their ecological, physiologicaland geographical requirements are remains virtually unknown.Here 1 summarize all reported cases of sympatry among six speciesof Cnemidophorus and discuss in detail specific examples ofsome of these interactions based on several years of field collectionsand observations. In addition I present the first field experimentalstudy designed to understand the ecological relationships ofsympatry in Cnemidophorus.     

Facultative parthenogenesis discovered in wild vertebrates

Facultative parthenogenesis (FP)—asexual reproduction by bisexual species—has been documented in a variety of multi-cellular organisms but only recently in snakes, varanid lizards, birds and sharks. Unlike the approximately 80 taxa of unisexual reptiles, amphibians and fishes that exist in nature, FP has yet to be documented in the wild. Based on captive documentation, it appears that FP is widespread in squamate reptiles (snakes, lizards and amphisbaenians), and its occurrence in nature seems inevitable, yet the task of detecting FP in wild individuals has been deemed formidable. Here we show, using microsatellite DNA genotyping and litter characteristics, the first cases of FP in wild-collected pregnant females and their offspring of two closely related species of North American pitviper snakes—the copperhead (Agkistrodon contortrix) and cottonmouth (Agkistrodon piscivorus). Our findings support the view that non-hybrid origins of parthenogenesis, such as FP, are more common in squamates than previously thought. With this confirmation, FP can no longer be viewed as a rare curiosity outside the mainstream of vertebrate evolution. Future research on FP in squamate reptiles related to proximate control of induction, reproductive competence of parthenogens and population genetics modelling is warranted.