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Evolutionary Dynamics and Consequences of Parthenogenesis in Vertebrates

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Evolutionary Dynamics and Consequences of Parthenogenesis in Vertebrates Annual Review of Ecology, Evolution, and Systematics Evolutionary Dynamics and Consequences of Parthenogenesis in Vertebrates Matthew K. Fujita,1 Sonal Singhal,2 Tuliana O. Brunes,3 and Jose A. Maldonado1 1Amphibian and Reptile Diversity Research Center and Department of Biology, University of Texas at Arlington, Arlington, Texas 76019, USA; email: [email protected] 2Department of Biology, California State University, Dominguez Hills, Carson, California 90747, USA 3Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo 05508-090, Brazil Annu. Rev. Ecol. Evol. Syst. 2020. 51:191–214 Keywords First published as a Review in Advance on parthenogenesis, sex, squamate, mutation, niche, asexual August 10, 2020 The Annual Review of Ecology, Evolution, and Abstract Access provided by CASA Institution Identity on 01/15/21. For personal use only. Systematics is online at ecolsys.annualreviews.org Parthenogenesis is asexual reproduction without any required participation Annu. Rev. Ecol. Evol. Syst. 2020.51:191-214. Downloaded from www.annualreviews.org https://doi.org/10.1146/annurev-ecolsys-011720- from males and, as such, is a null model for sexual reproduction. In a com- 114900 parative context, we can expand our understanding of the evolution and Copyright © 2020 by Annual Reviews. ecology of sex by investigating the consequences of parthenogenesis. In this All rights reserved review,we examine the theoretical predictions of and empirical results on the evolution of asexual reproduction in vertebrates, focusing on recent studies addressing the origins and geographic spread of parthenogenetic lineages and the genomic consequences of an asexual life history. With advances in computational methods and genome technologies, researchers are poised to make rapid and significant progress in studying the origin and evolution of parthenogenesis in vertebrates, thus providing an important perspective on understanding biodiversity patterns of both asexual and sexual populations. 191 INTRODUCTION Sex, reproduction that involves the fusion of recombinant gametes from distinct individuals, is foundational to multiple scientific and social disciplines, including human sexuality, demographics, sexual selection, reproduction biology, and development. Sexual reproduction is also ubiquitous across the tree of life. Thus, sex is a fundamental cellular mechanism, and understanding the ori- gins and evolution of sexual reproduction continues to be a major goal in biology. Paradoxically, some of the best insights into understanding sex come from examining the evolution of asex- ual populations, in which individuals clone themselves from one generation to the next. Indeed, multiple theoretical and empirical studies have addressed the long-term evolutionary advantages of sex over asexual reproduction (reviewed in Otto 2009, Otto & Lenormand 2002), the most prominent of which are increased adaptive potential because of recombination and the purging of deleterious variants (Maynard-Smith 1978, Muller 1964). However, sex suffers a severe, twofold demographic disadvantage compared with asexual reproduction: Because asexual populations do not need to produce males, asexual populations can grow exponentially faster than sexual popula- tions (Maynard-Smith 1978). Thus, for the long-term advantages to manifest, sexual populations must overcome the short-term demographic advantage of asexual populations (Figure 1). In this review, we discuss the evolutionary, genomic, molecular, and ecological mechanisms that influence the origin and evolution of asexual reproduction in vertebrates with the goal of understanding the dominance of sexual reproduction. Short-termTIME Long-term Asexual Asexual Benefits of Sexual Sexual individual sexual Mutations per reproduction Time Mites Genetic diversity Natural selection (Red Queen) Benefits of asexual Access provided by CASA Institution Identity on 01/15/21. For personal use only. reproduction Annu. Rev. Ecol. Evol. Syst. 2020.51:191-214. Downloaded from www.annualreviews.org Population growth Population growth (if still extant) Figure 1 The benefits of sexual and asexual reproduction at both short-term and long-term scales theoretically apply to all organisms, thoughwe demonstrate them here using lizards. Sex provides immediate benefits to a population because of standing genetic variation, which isan important contributor to adapting to rapidly changing environments, such as the involvement of frequency-dependent selection in host–parasite relationships. For example, greater genetic variation in sexual populations could provide resistance to parasites, such as mites, while asexual populations lack the diversity for that protection. Long-term benefits of sexual reproduction are centered around the efficacy of natural selection, allowing sexual populations to purge deleterious mutations but causing asexual populations to accumulate them. Asexual reproduction has an immediate demographic advantage, as populations can double with each generation. However, asexual reproduction has few, if any, advantages in the long term, and these populations will eventually go extinct. 192 Fujita et al. Despite its rarity, asexual reproduction occurs across the tree of life by several distinct mech- anisms. Parthenogenesis is a form of asexual reproduction by which females clone themselves without any contribution from males. This contrasts with other modes of vertebrate asexual repro- Parthenogenesis: duction exhibited by some fish, salamanders, and frogs, which require sperm to either(a) activate a mode of asexual egg maturation (gynogenesis), (b) contribute to the zygote’s genome (hybridogenesis, in which the evolution in which paternal genomic complement is subsequently excluded during gametogenesis), or (c) occasionally females clone contribute to the gene pool of asexual populations (kleptogenesis) (Avise 2008). Squamates (lizards themselves without and snakes) are the only vertebrates that reproduce via true parthenogenesis and thus maintain any contribution from males all-female populations. Facultative parthenogenesis occurs when a typically sexual organism re- produces without mating; such offspring may or may not be clones. Species of water fleas (Daphnia) Gynogenesis: a mode are perhaps the best-known examples in which populations alternate between sexual and faculta- of asexual evolution in which females clone tive parthenogenetic reproductive modes (reviewed in Decaestecker et al. 2009). However, several themselves but require lizards and snakes also exhibit facultative parthenogenesis, with cases often observed in captivity sperm to fertilize the when mateless females lay viable eggs (e.g., Miller et al. 2019, Watts et al. 2006) or even in wild egg; the sperm populations (Booth et al. 2012). Lineages that exhibit obligate parthenogenesis, the subject of this provides no genomic review, reproduce asexually with no contributions from sex. contribution but completes the egg’s Although representing only 0.6% of lizard and snake diversity, obligate parthenogenetic lin- maturation eages have arisen independently and multiple times in nine families across the squamate tree of life, providing natural and replicate experiments with which to study the evolution of asexuality Hybridogenesis: a mode of asexual in vertebrates (Kearney et al. 2009, Neaves & Baumann 2011, Sites et al. 2011). Some of the more evolution in which intensely studied groups include the whiptail lizards (Aspidoscelis), rock lizards (Darevskia), and sev- females require eral groups of geckos (Lepidodactylus and Heteronotia), although other systems, such as Gymnoph- fertilization for egg thalmidae: Loxopholis (Brunes et al. 2019) and Iguanidae: Liolaemus parthenos (Abdala et al. 2016), maturation, but the are beginning to provide important insights into the evolution of parthenogenesis. male genome is subsequently removed As the only truly parthenogenetic vertebrates (and the only amniote group with obligate asex- during gametogenesis ual lineages), squamates provide exceptional systems for investigating the consequences of asexu- in the offspring ality on vertebrate populations and genomes. Parthenogenetic squamates invariably have hybrid Kleptogenesis: origins: divergent, sexual progenitors hybridized to produce female offspring capable of clonal a mode of asexual reproduction (Figure 2). Parthenogenetic lineages thus have a perpetually hybrid genome, com- evolution in which posed of at least one complement from each parental species. Furthermore, backcrossing with females require one of the parentals, or even a third species, can result in triploid parthenogens (Figure 2). More fertilization for egg rarely, tetraploidy has been observed in natural populations (Danielyan et al. 2008, Moritz 1984), maturation, and the male genome can although recent hybrid parthenogens were produced and maintained in the laboratory, confirm- contribute to the gene ing that stable tetraploid lineages can be established (Cole et al. 2017, Lutes et al. 2011). Thus, pool of the asexual the genomes of parthenogenetic squamates are quite complex. In addition to being asexual, their population Access provided by CASA Institution Identity on 01/15/21. For personal use only. hybrid and sometimes polyploid nature requires the cooperation of divergent genomic comple- Annu. Rev. Ecol. Evol. Syst. 2020.51:191-214. Downloaded from www.annualreviews.org ments and perhaps some regulation to mediate gene dosage, as seen in gynogenetic Ambystoma salamanders (McElroy
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