PAPER Evolutionary perspectives on clonal reproduction in COLLOQUIUM vertebrate animals John C. Avise1 Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697 Edited by Francisco J. Ayala, University of California, Irvine, CA, and approved March 13, 2015 (received for review January 27, 2015) A synopsis is provided of different expressions of whole-animal aquarium fishes (9), to house pets (10, 11) and farm animals (12, vertebrate clonality (asexual organismal-level reproduction), both 13), and even to some to endangered species (14, 15). Although in the laboratory and in nature. For vertebrate taxa, such clonal NT cloning of humans (Homo sapiens) proved to be technically phenomena include the following: human-mediated cloning via somewhat more difficult, the ethically fraught task of cloning artificial nuclear transfer; intergenerational clonality in nature via human cells was finally accomplished in 2013 (16). parthenogenesis and gynogenesis; intergenerational hemiclonal- The line between artificial and natural cloning sometimes ity via hybridogenesis and kleptogenesis; intragenerational clon- blurs because nature in effect also deploys NT cloning occa- ality via polyembryony; and what in effect qualifies as clonal sionally, as for example under parthenogenesis when an egg cell replication via self-fertilization and intense inbreeding by simul- receives an unreduced nuclear genome and begins to proliferate taneous hermaphrodites. Each of these clonal or quasi-clonal mitotically into a daughter organism that is genetically identical mechanisms is described, and its evolutionary genetic ramifica- to her mother. The demarcation between artificial and natural tions are addressed. By affording an atypical vantage on standard cloning can blur even further when we take into account the fact vertebrate reproduction, clonality offers fresh perspectives on the that, for several vertebrate taxa, researchers occasionally have evolutionary and ecological significance of recombination-derived induced parthenogenesis, gynogenesis, hybridogenesis, or poly- genetic variety. embryony by various experimental procedures, such as forced hybridization, exposure to UV radiation or exotic chemicals, cloning | asexuality | unisexuality | parthenogenesis | polyembryony microsurgical embryonic splitting, or intense inbreeding in the EVOLUTION laboratory (3). s these symposium proceedings will attest, clonal reproduction Ais widely recognized to be an important component of the Unisexual Vertebrates and Intergenerational Clonality in reproductive repertoires in many pathogenic microbes, plants, Nature and invertebrate animals (1). Less widely appreciated is the fact About 100 “species” of vertebrate animal are known to consist that various expressions of clonal phenomena also occur in the solely of females who produce daughters that are genetically vertebrate realm, both under human and natural auspices. Here identical (barring de novo mutations) to one another and to their I briefly summarize research on the many varied manifesta- mother. Such an all-female taxon may not qualify as a biological tions of clonal and quasi-clonal reproduction (as defined in species in the usual sense of that term, because it is not held Box 1) by animals with backbones. The findings are of bi- together by the anastomotic bonds of mating that otherwise ological interest in their own right and are also relevant to our apply to standard bisexual species. Thus, the phrase “unisexual broader understanding of the ecological and evolutionary sig- biotype” (rather than species) is typically applied to male-absent nificance of alternative reproductive modalities. For more com- taxa that reproduce without benefit of sex. These unisexual prehensive treatments of clonal phenomena in vertebrate animals, biotypes reproduce via parthenogenesis (virgin birth), gynogen- readers are directed to refs. 2–4. esis, or hybridogenesis, all of which therefore constitute inter- generational expressions of clonality or hemiclonality. Black and Vertebrate Clonality Under Human Auspices white drawings of many of these species can be found in ref. 3. Beginning in the early 1950s, embryologists working with frogs developed laboratory techniques by which they could micro- Constitutive Parthenogenesis. All of the known vertebrate practi- surgically transfer the intact nucleus from a somatic cell of a tioners of constitutive (consistent) parthenogenesis reside in the tadpole or adult frog into an artificially enucleated frog egg (5, taxonomic order Squamata (lizards, snakes, and allies). Exam- Darevskia 6). Such nuclear transplantation (NT) experiments yielded egg ples include several rock lizards (especially in the genus ) cells that began to divide and multiply mitotically, eventuating in of the family Lacertidae (17), various geckos in the family Gekkonidae (18), whiptail lizards (especially in the genus Aspi- a new generation of offspring each of which was a clonal replica doscelis of its nuclear-donor parent. Evidently, under some circum- ) of the family Teiidae (19), skinks in the family Scincidae stances, the nuclear genome from a differentiated donor cell (20), and a blind snake in the family Typhlopidae (21). For each could begin to act again like a totipotent stem cell to direct full such unisexual biotype, reproduction transpires when a female embryonic development. These experiments surprised nearly produces chromosomally unreduced eggs that then proliferate everyone, because previously it was supposed that the genome of mitotically to form daughter individuals that display the same a liver cell (for example) had undergone tissue-specific changes in gene regulation that would have caused it to lose its pluri- potency (capacity to give rise to many different cell types in a This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “In the Light of Evolution IX: Clonal Reproduction: Alternatives to Sex,” held growing individual). In 2012, John Gurdon was awarded a Nobel January 9–10, 2015, at the Arnold and Mabel Beckman Center of the National Academies Prize in Physiology or Medicine for his pioneering role in stem- of Sciences and Engineering in Irvine, CA. The complete program and video recordings of cell research and NT cloning. most presentations are available on the NAS website at www.nasonline.org/ILE_IX_ In 1997, Wilmut et al. (7) extended NT cloning to another Clonal_Reproduction. vertebrate species when they produced the famous lamb Dolly, Author contributions: J.C.A. wrote the paper. the world’s first NT-generated mammalian clone. Since that The author declares no conflict of interest. time, researchers have NT cloned a wide variety of domestic and This article is a PNAS Direct Submission. other backboned animals, ranging from laboratory mice (8) and 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1501820112 PNAS | July 21, 2015 | vol. 112 | no. 29 | 8867–8873 Downloaded by guest on October 1, 2021 genetic constitution as the mother. No males or paternal gametes Kleptogenesis. A few unisexual vertebrate biotypes in nature do (sperm) are required to complete this strictly clonal operation. not fit easily into the categories parthenogenesis, gynogenesis, or hybridogenesis. Members of the salamander genus Ambystoma Facultative Parthenogenesis. In recent years, several instances of provide prime examples (35). So too do some ranid frogs (36). sporadic parthenogenesis (tychoparthenogenesis) have come to For some of these populations, genetic markers reveal that the light in species that otherwise reproduce sexually. For example, in unisexual biotypes sometimes incorporate bits of nuclear DNA the Burmese snake, Python molurus (22), and in the Bonnethead from locally sympatric sexual species into their diploid or poly- shark, Sphyrna tiburo (23), captive specimens without known ac- ploid nuclei. In other words, such otherwise clonal taxa appear to cess to males occasionally have given virgin birth to progeny that capture or “steal” some nuclear DNA from local congeners. have proved on molecular examination to be genetically identical Some of these hybridogenetic systems have also been described “ ” to their one and only female parent. I strongly suspect that many as genetically leaky. The mechanistic routes to such genomic additional instances of tychoparthenogenesis (either meiotic or thievery in these or other such taxa are not entirely clear, but the ameiotic) have gone unnoticed in nature simply because suitable mere fact that kleptogenetic (37) biotypes exist highlights the molecular markers have not been systematically deployed to ad- notion that some unisexual vertebrates are not strictly clonal dress possible clonal identities in large numbers of individuals or hemiclonal but instead probably gain some genetic benefits from most natural vertebrate populations. from occasional recombinational sex. The fact must be borne in mind when assessing the apparent evolutionary durations of Gynogenesis. This reproductive mode is quite like constitutive particular forms of clonal or quasi-clonal reproduction. parthenogenesis except that a sperm cell is required to activate Evolutionary and Genetic Origins. Without exception, all unisexual or stimulate mitotic divisions in each unreduced egg such that vertebrate biotypes arose via interspecific hybridization. The embryonic development ensues to produce a daughter that again species that hybridized to produce the parthenogens, gynogens, is clonally identical