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Viviparity and oviparity: Evolution and reproductive strategies

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Abstract

Viviparity is a reproductive pattern in which females retain developing eggs inside their reproductive tracts or body cavity and give birth to offspring capable of a free-living existence. Oviparity, in contrast, is a pattern in which females deposit eggs that develop and hatch in the external environment. These patterns can be viewed as "reproductive strategies," patterns that have advantages as well as disadvantages that affect their evolution. An advantage of viviparity, for example, is that embryos are protected and physiologically maintained by the pregnant female. In many viviparous species, the mother provides nutrients to the embryo during gestation, a pattern known as "matrotrophy." Viviparity has originated on over 160 times among animals and is found among bony fishes, cartilaginous fishes, amphibians, mammals, and squamate reptiles, as well as in several invertebrate groups. Viviparity and matrotrophy are phenomena of considerable biological interest. They have been studied from the standpoints of morphology, physiology, endocrinology, ecology, and evolution.
... Animal viviparity has evolved independently over 160 times, including 142 instances of convergent evolution amongst vertebrates (Blackburn 1999(Blackburn , 2015b. Given the diversity of conditions currently experienced by viviparous taxa, it is not clear which selective force, or forces, promoted viviparity in the first place. ...
... Given the diversity of conditions currently experienced by viviparous taxa, it is not clear which selective force, or forces, promoted viviparity in the first place. This mode of reproduction confers a variety of demonstrated or suspected fitness benefits, several of which have been proposed as the primary forces driving its evolution (Blackburn 1999), yet each tends to be relevant only in some of the viviparous taxa, and thus, we lack a unifying theoretical framework for the evolution of animal viviparity and matrotrophy (embryonic nutrition via maternal resources other than yolk; Table 1, see Supplementary Information). Here, we attempt to fill this gap in relation to vertebrate viviparity. ...
... Both gradualist (Blackburn 1992;Whittington et al. 2022) and saltationist models (Blackburn 1995) have been proposed to explain the evolution of viviparity and placentation. Yet neither gradual nor rapid transition from oviparity to matrotrophic viviparity would have been possible without the evolution of 1) the initial acquisition of internal fertilisation and egg retention, which seem to be a pre-requisite for the evolution of viviparity sensu stricto (Blackburn 1999), followed by 2) internal embryonic development within typically the female reproductive tract, where embryos are nourished only with nutrients contained in the vitellum (yolk) of the ovum (Blackburn 2000). Subsequently, 3) a lengthening of developing time (extended uterine gestation) matched by an increasing supplementation of nutrients released by the mother into her reproductive tract (incipient matrotrophic viviparity), and culminating, in some cases, in what we know as 4) matrotrophic viviparity (Blackburn 2000), where instead of yolk, nutrients are gradually provided by the mother in the form of oviductal secretions or through placental organs (see Supplementary Information). ...
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Viviparity has evolved from oviparity approximately 142 times among vertebrates. Different theories have been proposed to explain the evolution of each of its traits in the different taxa. None, however, is applicable to all the viviparous vertebrates, since the derived ecological advantages such as controlling incubating temperature or protecting eggs against predation differ amongst clades. Most theories have been developed under a co-adaptive perspective, whereas less attention has been paid to conflict. We developed a broad panorama of the gradual evolution, from oviparity to advanced forms of viviparity, that includes the different environmental and co-adaptive selective pressures that have been suggested to be at the root of the different instances of viviparity and of the diverse maternal–foetal adaptations for nutrient transfer seen amongst vertebrates. Furthermore, we highlight the importance of conflict as a crucial driver of the evolution of many of those traits, including the evolution of epigenetic control of maternal resources. We suggest that the different types of matrotrophic viviparity, and probably also some reversals to oviparity, have been the result of an antagonistic coevolution between mothers, fathers and offspring, and their genomes. We additionally suggest that the appearance of a trait that allowed or favoured the evolution of internal development and matrotrophy generates a new selective environment that promotes further adaptations or counteradaptations, leading to the observed diversity of forms of embryonic development, nourishment, and transfer of maternal nutrients, and ultimately to the diversity of extant viviparous taxa.
... Diverse solutions evolved for protecting developing youth across the tree of life; all these share nursing and protective mechanisms that optimize the individual's nutritional investment per propagule. Examples include placentation (Roberts et al., 2016), viviparity and matrotrophy in animals (Blackburn, 1999) or the seed in embryophytes (Goldberg et al., 1994). Many such traits are considered key innovations that spurred diversification (e.g., viviparity in fishes, Helmstetter et al., 2016), have arisen convergently (e.g., viviparity occurred~150 times in vertebrates (Blackburn, 2015), or underscore the evolutionary success of clades (e.g., seed plants, Westoby and Rice, 1982, but see Vamosi et al., 2018). ...
... Innovations in reproductive ability influence the evolutionary success of species (Heard and Hauser, 1995); consequently various solutions exist to protect developing youth, including nursing and protective mechanisms (Blackburn, 1999;Roberts et al., 2016). Animals evolved strategies for parental care, such as viviparity that increased the net diversification rate of the lineages (Helmstetter et al., 2016;Pyron and Burbrink, 2014), however, how general these are among other organisms is not known. ...
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The protection of vulnerable developing structures evolved repeatedly in terrestrial organisms and includes, among others, viviparity in animals and the seed in land plants. In mushroom-forming fungi (Agaricomycetes), sexual spores are born on fruiting bodies, the growth of which is a complex developmental process that is exposed to environmental factors (e.g., desiccation, fungivorous animals). Mushroom-forming fungi evolved a series of innovations in fruiting body protection, however, how these emerged is obscure, leaving the evolutionary principles of fruiting body development poorly known. Here, we show that developmental innovations that lead to the spore-producing surface (hymenophore) being enclosed in a protected environment display asymmetry in their evolution and are associated with increased diversification rates. ‘Enclosed’ development evolved convergently and became a dominant developmental type in several clades of mushrooms. This probably mirrors spore production benefits for species with protected fruiting body initials, by better coping with environmental factors. Our observations highlight new morphological traits associated with mushroom diversification that parallel the evolution of protection strategies in other organisms, such as viviparity or the seed in animals or plants, respectively, but in the context of spore development, highlighting the general importance of protecting vulnerable progeny across the tree of life.
... Due to their diurnal vertical migrations, they transfer large amounts of energy through the water column (Irigoien et al. 2014). In terms of reproduction, most mesopelagic fish are r-strategists producing small pelagic eggs (Blackburn 1999;Caiger et al. 2021) and their planktonic larval stages usually inhabit the epipelagic waters (Richards 2006;Olivar and Beckley 2022), where they can be collected with ichthyoplankton sampling gears (Cuttitta et al. 2004;Torres et al. 2011;Daudén-Bengoa et al. 2019). ...
Article
Full text is available at https://rdcu.be/c3kH7 Ichthyoplankton surveys hold much potential for studying fish biodiversity, but challenges and uncertainties in identification of early life stages and the drifting of planktonic eggs and larvae limit the efficacy of this method. In this study, we investigate mesopelagic fish biodiversity in Antalya Bay in the Northeastern Mediterranean Sea, based on ichthyoplankton samplings in combination with integrative taxonomy and particle backtracking simulations to overcome the forementioned limitations. We morphologically identified early life stages of 26 mesopelagic species and the identification of 17 of them was validated using DNA barcoding. With 13 species identified, Myctophidae was the most diverse family. Larvae of Cyclothone braueri Jespersen & Tåning, 1926, Diaphus holti Tåning, 1918, Ceratoscopelus maderensis (Lowe, 1839) and Cyclothone pygmea Jespersen & Tåning, 1926, constituted the most dominant species in the study area. Based on larval samples, we provided the first record of Paralepis coregonoides Risso, 1820, the first substantiated records of Vinciguerria poweriae (Cocco, 1838) and Hygophum hygomii (Lütken, 1892) and the second record of Evermannella balbo (Risso, 1820) off the Turkish coasts of the Mediterranean Sea. Particle backtracking simulations revealed that the spawning grounds of these species were in Antalya Bay, suggesting that there were reproducing populations of these species off the Mediterranean coast of Turkey, although these were not properly documented before the present study. Our results demonstrate that ichthyoplankton surveys can provide a reliable practice to study the biodiversity of understudied and difficult to access fish groups when combined with molecular identification techniques and particle backtracking simulations.
... Oviparous species release their gametes in the water column, where, after fertilization, the embryos will develop. Gametes and embryos in the water column are susceptible to predators, microbes, flooding, dehydration, ultraviolet light, and extreme temperatures (Blackburn, 1999). Asexual reproduction, in this case, might be an essential reproductive strategy because buds can develop into fully functional and independent individuals, growing fast, carrying the parent's genotype, and increasing the reproductive output and survival of the population (Singh & Thakur, 2015). ...
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Environmental factors are constantly changing in the intertidal region. Consequently, the various benthic organisms that densely colonize this ocean area had to adapt to these constant changes. Reproductive strategy might be considered one of these adaptations. However, knowledge about this aspect of the biology of marine invertebrates is still contentious for some groups, especially with regard to sponges (Porifera). Here, we investigated the effects of different environmental factors on the timing and effort of sexual and asexual reproduction in Cinachyrella apion and Tethya maza, two oviparous demosponges in Salvador, Bahia, Brazil. We analyzed the influence of humidity, atmospheric temperature, seawater temperature, photoperiod, rainfall, height of low tides, and chlorophyll‐a concentration on the density and size of oocytes and buds of these sponges. Both species reproduced aperiodically. Cinachyrella apion had a maximum 2.8 ± 4.04 oocytes/mm2 and 0.73 ± 0.15 buds/mm2, whereas T. maza had a maximum 6.0 ± 12.21 oocytes/mm2 and 0.31 ± 0.13 buds/mm2. The density of oocytes in C. apion was positively influenced by chlorophyll‐a concentration, whereas that of T. maza was negatively modulated by relative humidity. We did not observe any relationship between the environmental factors and bud density in C. apion, but bud density variation in T. maza was positively related to chlorophyll‐a concentration and to seawater temperature. It seems that individuals of both species alternated between the production of sexual and asexual propagules, suggesting a trade‐off between reproductive modes. Therefore, asexual and sexual reproduction seems to impact population growth and reproduction of both species, likely contributing to the recruitment of new sponges. In tropical intertidal regions, multiple environmental factors seem to contribute more to determining the quantity of sexual and asexual reproductive elements rather than the species' reproductive period.
... This event is well studied in placental mammals, possibly as one of the most innovative developmental phases of intrauterine retention of the fetus (Wagner et al. 2014). It also occurs in numerous species of reptiles, some amphibians, insects, and a few fish (Blackburn 1999). In a viviparous organism, the embryo develops inside the maternal tissue from which it obtains nourishment, rather than inside an egg (oviparity), which protects and nurtures the embryo outside the mother corpus. ...
Article
This review examines the historical research progress and areas of vivipary currently investigated in the Cactaceae. Vivipary, a rare attribute, has evolved multiple times in numerous plant lineages; however, a complete understanding of this event is still lacking in the cactus family and plants, in general. This literature search combines the results obtained from scientific sources addressing aspects of vivipary published since 1900 to 2000, with an emphasis from 2000 to 2021. This systematic compendium summarizes findings in various aspects of vivipary, such as the taxonomic and ecological range, offspring survival, and the physiological bases of this phenomenon in the Cactaceae. To date, 77 viviparous taxa circumscribed in subfamilies Pereskioideae and Cactoideae are known, representing approximately 5.4% vivipary at the family level. The taxonomic and geographic occurrence of this facultative reproductive attribute is discussed along with new reports, subsistence of viviparous and non-viviparous progeny, and a framework examining the phylogenetic distribution and putative origin of this generative mode in the family. The portrayal of the geographic distribution of viviparous species highlights the ubiquity of this trait and identifies vivipary hot spots in Cuba, the Brazilian Mata Atlântica, and NW Mexico, emphasizing ideas for cactus conservation. New data dealing with the role of the phytohormones abscisic acid and gibberellic acid in vivipary is examined in conjunction with the thermoregulatory properties of the fleshy viviparous fruits. Research areas deserving further studies are examined and several model species to conduct multidisciplinary research related to cactus vivipary in different areas of the Americas are proposed. Sharable link at: https://rdcu.be/cVUvF
... Parental care, a behavior enhancing offspring survival, evolved independently over 30 times (Mank et al. 2005;Wootton and Smith 2014) in teleost fishes ranging from nest guarding to live bearing (Wootton and Smith 2014). Most fish species are egg laying with external fertilization, whereas substantially fewer species (∼2%) are viviparous with internal fertilization and internal bearing (Blackburn 1999;Grier and Uribe 2005;Mank et al. 2005;Wootton and Smith 2014). Only a few species carry their eggs externally, which is called external bearing (Wootton and Smith 2014). ...
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The evolution of complex phenotypes like reproductive strategies is challenging to understand as they often depend on multiple adaptations, which only jointly result in a specific functionality. Sulawesi ricefishes (Adrianichthyidae) evolved a reproductive strategy termed pelvic brooding. In contrast to the more common transfer brooding, female pelvic brooders carry an egg‐bundle connected to their body for weeks until the fry hatches. To examine the genetic architecture of pelvic brooding, we crossed the pelvic brooding Oryzias eversi and the transfer brooding O. nigrimas (species divergence time: ∼ 3.6 my). We hypothesize, that a low number of loci and modularity have facilitated the rapid evolution of pelvic brooding. Traits associated to pelvic brooding, like rib length, pelvic fin length and morphology of the genital papilla were correlated in the parental species but correlations were reduced or lost in their F1 and F2 hybrids. Using the Castle‐Wright estimator, we found that generally few loci underlie the studied traits. Further, both parental species showed modularity in their body plans. In conclusion, morphological traits related to pelvic brooding were based on a few loci and the mid‐body region likely could evolve independently from the remaining body parts. Both factors presumably facilitated the rapid evolution of pelvic brooding. This article is protected by copyright. All rights reserved
... The interest of studying them is twofold. First, as they represent the majority of species (Blackburn, 1999), it is important to understand these effects in order to protect and preserve these species. Second, because their embryos develop outside a maternal organism, their prenatal environment can be better controlled. ...
Article
As the sensory systems of vertebrates develop prenatally, embryos perceive many environmental stimuli that can influence the ontogeny of their behaviour. Whether the nature and intensity of prenatal stimuli affect differently this ontogeny remains to be investigated. In this context, this study aimed to analyse the effects of prenatal auditory stimulations (natural stimulations “NS”: predator vocalisations, or artificial stimulations “AS”: metallic sounds) on the subsequent behaviour of young Japanese quail (Coturnix coturnix japonica). For that, behavioural variables recorded during ethological tests evaluating emotional and social reactivity were analysed using a principal component analysis. This analysis revealed significant differences between the behavioural profile of stimulated chicks and that of non-exposed chicks. Indeed, chicks exposed to NS expressed more intense emotional responses in fearful situations, but less neophobia in the presence of a novel environment or object, whereas chicks exposed to AS appeared more sensitive to social isolation. Our original results show that the acoustic environment of embryos can influence the way young birds subsequently interact with their social and physical environment after hatching, and face challenges in changing living conditions.
... gives birth to offspring hatched from the eggs. Viviparous animals develop offspring from the eggs and give 7 birth to offspring capable of free-living (Blackbum, 1999). The body's internal environment of animals is more 8 stable than the external environment, especially for endothermic animals (Kvarnemo & Forsgren, 2000;Canals, 9 1998). ...
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Avian reproduction has four prime components: nesting, mating, hatching, and fledging. Predicting the probability of individual components helps in identifying the period of reproduction that would benefit from an increased conservation effort. Identification of biotic, abiotic, and sociological variables of the nesting sites is essential to calculate the component-wise success probabilities. There is no standard methodology to estimate these probability values separately. This study proposes a methodology to estimate the success probability of each component, identifies correlated environmental predictors, and provides a modelling framework to accurately predict the nesting success probabilities using Merops philippinus as a model species. Primary surveillance data and the proposed methodology indicate that the time window between the bird's nesting and mating is most vulnerable to environmental fluctuations. Both biotic and abiotic factors are crucial determinants of nesting success. Sociological factors also play a crucial role in determining the probabilities of these successes. Mating, hatching, and fledging success depend more on biotic factors than abiotic ones. Linear modelling frameworks are helpful in exploring which types of environments are better determinants of the success of a reproductive component. Artificial neural networks are useful in predicting mating, nesting, and overall reproductive success probabilities. Though the models in this study are developed using Merops philippinus data, the proposed methodology and modelling framework is also applicable for other bird species.
... The reproductive strategies of oviparity and viviparity both entail advantages and disadvantages, each of which may differ in their applicability to particular species. The universality of internal fertilization in reptiles readily permits the evolution of viviparity which evolved over 100 times in different lineages of the order Squamata, often at subfamilial and subgeneric levels and, in some cases, at the subspecific level (Blackburn, 1999). From the standpoint of life history theory viviparity should evolve only when the benefits of stages that are evolutionarily intermediate outweigh the costs. ...
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In a captive colony of Chersina angulata in Cape Town, South Africa, we observed in 2015/16 retention of the last egg clutch inside the female until the hatching stage was reached, conforming to the generally accepted definition of viviparity. Retrospective climatic analysis indicates egg retention until the hatching stage co-occurred with unusually hot summer weather: the average air temperatures in December 2015 and January and February 2016 were higher than during the preceding five and the following 5 years when facultative viviparity could not be observed. Late December and January appears to be the critical period for females to either deposit their last clutch of the nesting season into a nest, or to retain the last clutch for embryonic development inside the female. Over the 28 December to 24 January period the minimum, average and maximum air temperatures in 2015–16 were about 3°C higher than in the five following years. This association of facultative viviparity with unusual summer heat suggests that hot ambient temperatures at the end of the nesting season may cue females to switch from oviposition to facultative viviparity. Compared to incubation in a nest this phenotypic plasticity of the reproductive mode—to retain during hot summers the season’s last clutch inside the female—may buffer the developing embryos from excessive heat exposure: females can thermo-regulate by moving among microhabitats whereas sun exposed shallow nests cannot escape high ground temperatures. This novel reproductive strategy has the potential to enhance the resilience of species to global warming.
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