PhD Student, University of California, Riverside
I study the evolutionary consequences of having a placenta using livebearing fishes.
Placentas are well-known reproductive organs in mammals used to nourish offspring in-utero. However, many non-mammalian organisms also possess placentas. Species in the livebearing fish family Poeciliidae have evolved placentas multiple times throughout evolutionary history. The presence or absence of a placenta in closely related species allows us to experimentally assess the biological consequences of having a placenta. Specifically, parent-offspring conflict is a predicted consequence of the inequalities between the quantity of resources in the best interest of mother to provide her offspring and the somewhat larger quantity that are in the best interest of offspring to get from their mother. This conflict is exaggerated if females mate with multiple males. Mothers in species that lack placentas fully provision eggs before fertilization. Parent-offspring conflict is predicted to be low because offspring cannot garner more resources from their mother than mothers provided before the egg was fertilized. Species with placentas are predicted to have high levels of conflict because mothers continue to supply nutrients throughout the development of their offspring. My experiment investigates parent-offspring conflict and genomic conflict between parents’ in closely related species with and without placentas. Conflict theory predicts that there will be a reconciliation of conflict within populations but differences among populations in how conflict is resolved. If so, females may be able to recognize and differentially allocate resources to offspring sired by males from her own population. I am providing females with sperm from males in their own population and a different population through artificial insemination. Then, I am looking at the resulting paternity of the offspring, as well as how many resources they were provided, by weighing them at birth. This project tells us how females allocate resources based on the male they are mating with, both in fertilizing eggs and in providing nutrients to their offspring.
Abstract: Equipped with Mendel's laws and only rudimentary knowledge of genes and genomes, the architects of the Modern Synthesis provided key insights into the dynamics of gene frequency change within populations. Extension of population genetic models to speciation identified Dobzhansky-Muller incompatibilities (negative epistatic interactions between genes from isolated populations) as the primary cause of hybrid inviability and sterility, a view consistent with empirical findings on the genetics of reproductive isolation in Drosophila. Although speciation models have become increasingly mathematically sophisticated, many remain based on an overly static concept of the genome, grounded in Mendelian genetics and devoid of potentially important biological details. A unifying theory of speciation therefore remains elusive, with debate over the relative importance of natural selection, sexual selection, sexual conflict, genetic drift, and selfish genetic elements in the evolution of reproductive isolation. Drawing on recent findings in molecular genetics and comparative genomics, we revisit, update, and extend the theory that reproductive mode plays a crucial role in shaping the speciation process. By providing a direct conduit for manipulation of the mother's physiology by genes expressed in the embryo, viviparity creates a postfertilization arena for genomic conflicts absent in species that lay eggs. In polyandrous species, viviparity-driven conflict (VDC) is likely to generate perpetual antagonistic coevolution between genes expressed during embryonic development and those involved in maternal reproductive physiology, thereby accelerating the rate at which postzygotic isolation evolves between populations. Moreover, in mammals and flowering plants, VDC has favored the evolution of genomic imprinting and a central role for epigenetic mechanisms in the regulation of antagonistic patterns of gene expression by maternally and paternally inherited genomes. VDC can account for the rapid rate at which mammals and viviparous fishes lose their ability to hybridize; the key role of the triploid endosperm in postzygotic reproductive isolation in flowering plants; and the kinds of traits, genes, and gene regulatory systems most critical to the evolution of postzygotic reproductive isolation in live-bearing species.
Pub.: 19 Jun '08, Pinned: 07 Jun '17
Abstract: In birds and frogs, species pairs retain the capacity to produce viable hybrids for tens of millions of years, an order of magnitude longer than mammals. What accounts for these differences in relative rates of pre- and postzygotic isolation? We propose that reproductive mode is a critically important but previously overlooked factor in the speciation process. Viviparity creates a post-fertilization arena for genomic conflicts absent in egg-laying species. With viviparity, conflict can arise between: mothers and embryos; sibling embryos in the womb, and maternal and paternal genomes within individual embryos. Such intra- and intergenomic conflicts result in perpetual antagonistic coevolution, thereby accelerating interpopulation postzygotic isolation. In addition, by generating intrapopulation genetic incompatibility, viviparity-driven conflict favors polyandry and limits the potential for precopulatory divergence. Mammalian diversification is characterized by rapid evolution of incompatible feto-maternal interactions, asymmetrical postzygotic isolation, disproportionate effects of genomically-imprinted genes, and "F(2) hybrid enhancement. " The viviparity-driven conflict hypothesis provides a parsimonious explanation for these patterns in mammalian evolution.
Pub.: 14 Sep '00, Pinned: 07 Jun '17
Abstract: Placentae show considerable diversity in a number of nonmammalian, viviparous organisms, including amphibians, reptilian sauropsids, teleost fish, and chondrichthyes. However, the evolutionary processes driving the evolution of placenta are still debated. In teleost fishes, the genus Poeciliopsis (Poeciliidae) offers a rare opportunity for studying placental evolution: extensive placentation has evolved three independent times within the last 750,000 years and there is substantial interspecific variation in the degree of embryonic, maternal nutrient provisioning and development of the placenta. In poeciliids, the placenta is composed of a hypertrophied maternal follicular epithelium apposed to a highly vascularized embryonic pericardial sac. To better understand placental evolution, we have undertaken a comprehensive comparative study of the maternal follicle in eight closely related Poeciliopsis species that span the range in postfertilization, embryonic, maternal nutrient provisioning (from lecithotrophs, to moderate matrotrophs, to extensive matrotrophs). Using light and scanning electron microscopy, we found that the species that provide extensive postfertilization maternal nutrient provisioning (extensive matrotrophs) have thicker follicles and more extensive folding of the follicular epithelium compared to the lecithotrophs and moderate matrotrophs. Follicle sections and histology revealed that epithelial folds of the extensive matrotrophs are comprised primarily of cuboidal and columnar cells and are richly supplied with capillaries. Among the extensive matrotrophs, enhancements of follicle traits corresponded with increases in the level of maternal nutrient provisioning. Hypertrophied maternal follicles with richly vascularized folds can serve to increase the surface area and, thus, facilitate the transfer of substances between the mother and developing embryo. Finally, we found egg envelopes in the lecithotrophs and moderate matrotrophs, but not in the extensive matrotrophs. Morphological studies, like this one, can provide a better understanding of the natural variation in the structure and functioning of maternal and offspring traits associated with matrotrophy and, thus, insights into the processes driving placental evolution. J. Morphol. 276:707-720, 2015. © 2015 Wiley Periodicals, Inc.
Pub.: 15 Mar '15, Pinned: 07 Jun '17
Abstract: Matrotrophic fish in the genus Poeciliopsis (Poeciliidae) have a placenta-like structure used in postfertilization maternal provisioning of the developing embryo. To understand better the structure and function of the Poeciliopsis placenta, we derived cDNA libraries from the maternal follicular placenta of 2 matrotrophic Poeciliopsis sister species, P. turneri and P. presidionis. These species inherited their placenta from a common ancestor and represent one of 3 independent origins of placentas in Poeciliopsis. Expressed sequence tags (ESTs) were generated and putative function was determined using BLASTX homology searches and Gene Ontology (GO) annotation. Reverse transcription-polymerase chain reaction was used to verify placenta tissue expression of a putative candidate gene, alpha-2 macroglobulin. In total, 1956 (71.5% of the total submitted ESTs) and 924 (71.0% of the total submitted ESTs) unique transcripts were identified for the P. turneri and P. presidionis placenta, respectively. Homology search and GO annotation revealed putative genes whose products may be involved in specific transport functions of the maternal follicle. These putative genes are excellent candidates for future research on the evolution of the placenta. We discuss our results in light of the parent-offspring conflict theory of placental evolution and in terms of the Poeciliid placenta structure and function.
Pub.: 23 Feb '11, Pinned: 07 Jun '17
Abstract: The evolution of complex organs is a source of controversy because they require the contributions of many adaptations to function properly. We argue that placentas are complex, that they have evolved multiple times in Poeciliopsis, and that there are closely related sister taxa that have either no placentas or intermediate stages in the evolution of a placenta. Furthermore, placentas can evolve in 750,000 years or less, on the same time scale as suggested by theoretical calculations for the evolution of complex eyes. Independent origins of such complexity, accompanied by sister taxa that either lack or have intermediate stages in the evolution of the trait, present an opportunity to study the evolution of novelty and complexity from a comparative, evolutionary perspective.
Pub.: 02 Nov '02, Pinned: 07 Jun '17
Abstract: Abstract Parents and children are genetically related, but they are not genetically identical. This difference leads to diverging interests and ensuing conflict. There are two, not mutual exclusive, hypotheses that propose to account for how the divergence in genetic interests leads to conflict over mating, namely the compromises in traits and the evolutionary trade-offs. The present paper attempts to demonstrate that the compromises in trait hypothesis can account for this conflict, but the evolutionary trade-off hypothesis cannot. It also aims to combine insights from the two hypotheses in order to provide a better account of the nature of parent-offspring conflict over mating. In the proposed synthesis, compromises in desirable traits lead to parent-offspring conflict over mating, with evolutionary trade-offs regulating the degree of this conflict depending on the sex of the child exercising mate choice and the local conditions.AbstractParents and children are genetically related, but they are not genetically identical. This difference leads to diverging interests and ensuing conflict. There are two, not mutual exclusive, hypotheses that propose to account for how the divergence in genetic interests leads to conflict over mating, namely the compromises in traits and the evolutionary trade-offs. The present paper attempts to demonstrate that the compromises in trait hypothesis can account for this conflict, but the evolutionary trade-off hypothesis cannot. It also aims to combine insights from the two hypotheses in order to provide a better account of the nature of parent-offspring conflict over mating. In the proposed synthesis, compromises in desirable traits lead to parent-offspring conflict over mating, with evolutionary trade-offs regulating the degree of this conflict depending on the sex of the child exercising mate choice and the local conditions.
Pub.: 27 Jul '16, Pinned: 07 Jun '17
Abstract: Parent-offspring conflict theory predicts the emergence of weaning conflict between a mother and her offspring arising from skewed relatedness benefits. Empirical observations of weaning conflict have not been carried out in canids. In a field-based study on free-ranging dogs we observed that nursing/suckling bout durations decrease, proportion of mother-initiated nursing bouts decrease and mother-initiated nursing/suckling terminations increase with pup age. We identified the 7th - 13th week period of pup age as the zone of conflict between the mother and her pups, beyond which suckling solicitations cease, and before which suckling refusals are few. We also report for the first time milk theft by pups who take advantage of the presence of multiple lactating females, due to the promiscuous mating system of the dogs. This behaviour, though apparently disadvantageous for the mothers, is perhaps adaptive for the dogs in the face of high mortality and competition for resources.
Pub.: 09 Feb '17, Pinned: 07 Jun '17
Abstract: We present a theory of the origin and evolution of infant-directed song, a form of music found in many cultures. After examining the ancestral ecology of parent-infant relations, we propose that infant-directed song arose in an evolutionary arms race between parents and infants, stemming from the dynamics of parent-offspring conflict. We describe testable predictions that follow from this theory, consider some existing evidence for them, and entertain the possibility that infant-directed song could form the basis for the development of other, more complex forms of music.
Pub.: 03 Jan '17, Pinned: 07 Jun '17
Abstract: Vertebrate viviparity (live-bearing reproduction), placentation, and placentotrophy are widely assumed to have evolved as three successive, gradualistic transformations. From empirical data and predictive tests on lizards and snakes, this paper indicates that placentae and a degree of placentotrophy have evolved repeatedly as necessary correlates of viviparity, not as subsequent modifications. In addition, information derived from studies of anatomy, physiology, biogeography and systematics is used to evaluate new saltationist and punctuated equilibrium models for the evolution of viviparity. Phylogenetic reconstruction reveals that more than 100 squamate clades have made the transition to viviparity and placentation. However, various phenotypic intermediates postulated by the gradualistic model are either scarce or unrepresented among known forms, including those in which viviparity has evolved at specific and subspecific levels. Evolution in squamates seems to have produced a dichotomy between two evolutionarily stable patterns: (i) retention of weakly shelled or shell-free eggs to term (viviparity), with development of fully functional placentae; and (ii) deposition of shelled eggs at or near the limb bud stage of development (typical oviparity). Conflicting functional demands placed on eggshell morphology may constrain establishment of prolonged, oviparous egg-retention as a viable, historically stable pattern. Alternatively, the costs of prolonged egg-retention associated with decreased female mobility or decreased fecundity may exceed the benefits in oviparous forms.
Pub.: 21 May '95, Pinned: 07 Jun '17
Abstract: A recent paper in J. theor. Biol. has challenged the proposed application of punctuated equilibrium models to the evolution of reptilian viviparity and placentation. While clarifying some aspects of the models, the paper's criticisms reflect misinterpretations of the literature and an unnecessary reluctance to apply punctuationist concepts to extant taxa. The punctuated equilibrium model retains potential for clarification of the patterns of stasis and episodic change that may well have characterized squamate reproductive history.Copyright 1998 Academic Press Limited
Pub.: 15 Sep '98, Pinned: 07 Jun '17
Abstract: Viviparity in squamate reptiles is widely recognized as having evolved convergently from oviparity more than 100 times. However, questions persist as to whether reversals from viviparity back to oviparity have ever occurred. Based on a theoretical model, a recent paper (Pyron and Burbrink, 2014) has proposed that viviparity is ancestral for squamates and that viviparity-oviparity reversals have far outnumbered origins of viviparity in reproductive history. Close examination of this analysis reveals features that cast doubt on its plausibility, notably the requirement of repeated, sequential transformations back and forth between these reproductive modes, as well as numerous, uncounted evolutionary transformations that have produced inaccurate estimates of parsimony. Evidence derived from studies of anatomy, physiology, and developmental biology strongly supports the inference that oviparity is ancestral for squamates and has given rise to viviparity on numerous occasions. Biological data provide important insights into the likelihood of evolutionary transformations, and deserve to be incorporated fully into future analyses of the evolution of reproductive modes.
Pub.: 15 May '15, Pinned: 07 Jun '17
Abstract: The expression pattern of genes in mammals and plants can depend upon the parent from which the gene was inherited, evidence for a mechanism of parent-specific genomic imprinting. Kinship considerations are likely to be important in the natural selection of many such genes, because coefficients of relatedness will usually differ between maternally and paternally derived genes. Three classes of gene are likely to be involved in genomic imprinting: the imprinted genes themselves, trans-acting genes in the parents, which affect the application of the imprint, and trnas-acting genes in the offspring, which recognize and affect the expression of the imprint. We show that coefficients of relatedness will typically differ among these three classes, thus engendering conflicts of interest between Imprinter genes, imprinted genes, and imprint-recognition genes, with probable consequences for the evolution of the imprinting machinery.
Pub.: 13 Mar '99, Pinned: 07 Jun '17
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