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"Reznick, D. N."
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The evolution of the placenta drives a shift in sexual selection in livebearing fish
2014
In poeciliid fish, the evolution of the placenta is associated with polyandry in females and correlates with a suite of phenotypic and behavioural traits in males.
Consequences of placenta evolution
Females laying eggs for external fertilization have no control over the quality of the offspring, and must rely on proxies of male quality such as courtship and display traits. Evolutionary theory holds that all this changed with the advent of the placenta: with low-cost eggs incubated internally, a mother can hedge her bets, inspecting the genetic quality of her mates directly and provisioning her embryos accordingly. The resulting mother–offspring conflict is expected to lead to polyandry (females mating with multiple males) and to males that are smaller, less showy and more prone to opportunistic or 'sneaky' mating. Here Bart Pollux
et al
. test these ideas by looking at the Poecilidae — guppies and their relatives — a family of fish in which the various species show all varieties of internal and external fertilization, and in which the placenta has evolved at least eight times independently. This approach allows the authors to confirm that the evolution of the placenta is associated with polyandry in females, and smaller, less showy males that have longer penises to facilitate more opportunities for opportunistic mating.
The evolution of the placenta from a non-placental ancestor causes a shift of maternal investment from pre- to post-fertilization, creating a venue for parent–offspring conflicts during pregnancy
1
,
2
,
3
,
4
. Theory predicts that the rise of these conflicts should drive a shift from a reliance on pre-copulatory female mate choice to polyandry in conjunction with post-zygotic mechanisms of sexual selection
2
. This hypothesis has not yet been empirically tested. Here we apply comparative methods to test a key prediction of this hypothesis, which is that the evolution of placentation is associated with reduced pre-copulatory female mate choice. We exploit a unique quality of the livebearing fish family Poeciliidae: placentas have repeatedly evolved or been lost, creating diversity among closely related lineages in the presence or absence of placentation
5
,
6
. We show that post-zygotic maternal provisioning by means of a placenta is associated with the absence of bright coloration, courtship behaviour and exaggerated ornamental display traits in males. Furthermore, we found that males of placental species have smaller bodies and longer genitalia, which facilitate sneak or coercive mating and, hence, circumvents female choice. Moreover, we demonstrate that post-zygotic maternal provisioning correlates with superfetation, a female reproductive adaptation that may result in polyandry through the formation of temporally overlapping, mixed-paternity litters. Our results suggest that the emergence of prenatal conflict during the evolution of the placenta correlates with a suite of phenotypic and behavioural male traits that is associated with a reduced reliance on pre-copulatory female mate choice.
Journal Article
Adaptive Versus Non-Adaptive Phenotypic Plasticity and the Potential for Contemporary Adaptation in New Environments
by
S. P. Carroll
,
J. K. Mc Kay
,
Reznick, D. N.
in
adaptive divergence
,
adaptive radiation
,
Biological adaptation
2007
1. The role of phenotypic plasticity in evolution has historically been a contentious issue because of debate over whether plasticity shields genotypes from selection or generates novel opportunities for selection to act. Because plasticity encompasses diverse adaptive and non-adaptive responses to environmental variation, no single conceptual framework adequately predicts the diverse roles of plasticity in evolutionary change. 2. Different types of phenotypic plasticity can uniquely contribute to adaptive evolution when populas are faced with new or altered environments. Adaptive plasticity should promote establishment and persistence in a new environment, but depending on how close the plastic response is to the new favoured phenotypic optimum dictates whether directional selection will cause adaptive divergence between populations. Further, non-adaptive plasticity in response to stressful environments can result in a mean phenotypic response being further away from the favoured optimum or alternatively increase the variance around the mean due to the expression of cryptic genetic variation. The expression of cryptic genetic variation can facilitate adaptive evolution if by chance it results in a fitter phenotype. 3. We conclude that adaptive plasticity that places populations close enough to a new phenotypic optimum for directional selection to act is the only plasticity that predictably enhances fitness and is most likely to facilitate adaptive evolution on ecological timescales in new environments. However, this type of plasticity is likely to be the product of past selection on variation that may have been initially non-adaptive. 4. We end with suggestions on how future empirical studies can be designed to better test the importance of different kinds of plasticity to adaptive evolution.
Journal Article
Do Faster Starts Increase the Probability of Evading Predators?
by
Walker, J. A.
,
Griset, O. L.
,
McKenney, D.
in
Agnatha. Pisces
,
Animal and plant ecology
,
Animal morphology
2005
1. Nearly all fish evade predation strikes by rapidly accelerating out of the strike path, a behaviour called the fast-start evasion response. The many studies investigating morphological, behavioural and ecological correlates of fast-start performance assume that faster starts increase the probability of evasion. 2. We tested this faster-start hypothesis by measuring the effect of acceleration ability on evasion outcome (success, failure) in Guppies (Poecilia reticulata) evading the strike of a natural predator, the Pike Cichlid (Crenicichla alta). 3. Four parameters affect evasion outcome: two parameters important to the predator-prey interaction but not to the faster-start hypothesis -- (1) the time required to reach the prey by the striking predator (measured by the initial distance between predator and prey and strike velocity), (2) the evasion path of the prey relative to the strike path of the predator; and two parameters relevant to the faster-start hypothesis -- (1) the ability of the prey to generate rapid tangential acceleration (measured by net distance travelled, maximum velocity, and maximum acceleration), and (2) the ability of the prey to rapidly rotate during the initial stage of the fast start. 4. On average, a one standard deviation increase in fast-start performance increases the odds of surviving a predation strike 2·3-fold. These results support the assumption that faster starts increase the probability of successfully evading a predation strike.
Journal Article
Evolution on ecological time-scales
by
REZNICK, D.N
,
CARROLL, S.P
,
HENDRY, A.P
in
anthropogenic activities
,
anthropogenic change
,
contemporary evolution
2007
1. Ecologically significant evolutionary change, occurring over tens of generations or fewer, is now widely documented in nature. These findings counter the long-standing assumption that ecological and evolutionary processes occur on different time-scales, and thus that the study of ecological processes can safely assume evolutionary stasis. Recognition that substantial evolution occurs on ecological time-scales dissolves this dichotomy and provides new opportunities for integrative approaches to pressing questions in many fields of biology. 2. The goals of this special feature are twofold: to consider the factors that influence evolution on ecological time-scales - phenotypic plasticity, maternal effects, sexual selection, and gene flow - and to assess the consequences of such evolution - for population persistence, speciation, community dynamics, and ecosystem function. 3. The role of evolution in ecological processes is expected to be largest for traits that change most quickly and for traits that most strongly influence ecological interactions. Understanding this fine-scale interplay of ecological and evolutionary factors will require a new class of eco-evolutionary dynamic modelling. 4. Contemporary evolution occurs in a wide diversity of ecological contexts, but appears to be especially common in response to anthropogenic changes in selection and population structure. Evolutionary biology may thus offer substantial insight to many conservation issues arising from global change. 5. Recent studies suggest that fluctuating selection and associated periods of contemporary evolution are the norm rather than exception throughout the history of life on earth. The consequences of contemporary evolution for population dynamics and ecological interactions are likely ubiquitous in time and space.
Journal Article
Evolution of Placentas in the Fish Family Poeciliidae: An Empirical Study of Macroevolution
by
Reznick, D.N.
,
Pires, M.N.
,
Pollux, B.J.A.
in
Agnatha. Pisces
,
Animal and plant ecology
,
Animal, plant and microbial ecology
2009
The placenta is a complex organ that mediates all physiological and endocrine interactions between mother and developing embryos. Placentas have evolved throughout the animal kingdom, but little is known about how or why the placenta evolved. We review hypotheses about the evolution of placentation and examine empirical evidence in support for these hypotheses by drawing on insights from the fish family Poeciliidae. The placenta evolved multiple times within this family, and there is a remarkable diversity in its form and function among closely related species, thus providing us with ideal material for studying its evolution. Current hypotheses fall into two categories: adaptive hypotheses, which propose that the placenta evolved as an adaptation to environmental pressures, and conflict hypotheses, which posit that the placenta evolved as a result of antagonistic coevolution. These hypotheses are not mutually exclusive. Each may have played a role at different stages of the evolutionary process.
Journal Article
Evaluation of the Rate of Evolution in Natural Populations of Guppies (Poecilia reticulata)
1997
Natural populations of guppies were subjected to an episode of directional selection that mimicked natural processes. The resulting rate of evolution of age and size at maturity was similar to rates typically obtained for traits subjected to artificial selection in laboratory settings and up to seven orders of magnitude greater than rates inferred from the paleontological record. Male traits evolved more rapidly than female traits largely because males had more genetic variation upon which natural selection could act. These results are considered in light of the ongoing debate about the importance of natural selection versus other processes in the paleontological record of evolution.
Journal Article
Do placental species abort offspring? Testing an assumption of the Trexler-DeAngelis model
by
Reznick, D. N.
,
Banet, A. I.
in
Animal and plant ecology
,
Animal reproduction
,
Animal, plant and microbial ecology
2008
1. We investigate how resource level affects reproduction in matrotrophic (Poeciliopsis prolifica) and lecithotrophic (P. monacha) fishes. 2. One of our goals was to test an assumption of the Trexler-DeAngelis model for the evolution of matrotrophy, which was that matrotrophic species can adjust litter size by aborting offspring in low food conditions. Our more general goal was to elucidate other differences between the reproductive modes. 3. Both species have superfetation and c. 30-day development time. Females of each species were assigned to high or low food availability for 30 days, or one gestation period. Any young born during that time interval would have initiated development before the initiation of the experiment. If embryos are aborted, then this would be seen as a reduction in brood size in the low food treatment relative to the high food treatment within this period. 4. Our results suggest P. monacha responds to low food by sacrificing reproduction to maintain lipids, while P. prolifica maintains reproduction at the expense of lipids. Neither species showed a significant reduction in offspring number over the course of the experiment, suggesting that these species do not abort offspring in low food conditions.
Journal Article
Heterochrony in the evolution of Trinidadian guppy offspring size: maturation along a uniform ontogenetic trajectory
by
Dial, T. R.
,
Reznick, D. N.
,
Brainerd, E. L.
in
Allometry
,
Animals
,
Animals, Newborn - growth & development
2017
The size and maturity of Trinidadian guppy (Poecilia reticulata) offspring vary among populations adapted to environments of differential predation. Guppy offspring born to low-predation, high-competition environments are larger and more mature than their high-predation ancestors. Here we ask: what specific changes in developmental or birth timing occur to produce the larger, more mature neonates? We collected specimens across the perinatal window of development from five populations and quantified musculoskeletal maturation. We found that all populations undergo similar ontogenetic trajectories in skeletal and muscle acquisition; the only difference among populations is when neonates emerge along the trajectory. The smallest neonates are born with 20% of their skeleton ossified, whereas the largest neonates are born with over 70% of their skeleton ossified. The area of the major jaw-closing muscle is relatively larger in larger offspring, scaling with length as L²·⁵. The size range over which offspring are birthed among populations sits along the steepest part of the size-maturity relationship, which provides a large marginal increase in fitness for the high-competition female. Because of the functional effects of producing more mature offspring at birth, offspring size may be the first and most critical life-history trait selected upon in highly competitive environments.
Journal Article
Constraints on Adaptive Evolution: The Functional Trade‐Off between Reproduction and Fast‐Start Swimming Performance in the Trinidadian Guppy (Poecilia reticulata)
by
Ghalambor, Cameron K.
,
Reznick, David N.
,
Walker, Jeffrey A.
in
Adaptation
,
Adaptation, Physiological
,
Animal behavior
2004
The empirical study of natural selection reveals that adaptations often involve trade‐offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life‐history evolution on locomotor performance in the live‐bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast‐start swimming performance to evade predators. Because embryo development increases a female’s wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast‐start performance. We find evidence for adaptive but constrained evolution of fast‐start swimming performance in laboratory trials conducted on second‐generation lab‐reared fish. Female guppies from high‐predation localities attain a faster acceleration and velocity and travel a greater distance during fast‐start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high‐ and low‐predation populations. This functional trade‐off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole‐organism level.
Journal Article
Pre- and Post-Fertilization Maternal Provisioning in Livebearing Fish Species and Their Hybrids (Poeciliidae: Poeciliopsis)
by
Pires, M. N.
,
Vrijenhoek, R. C.
,
Turcotte, M. M.
in
Agnatha. Pisces
,
Animal and plant ecology
,
Animal, plant and microbial ecology
2008
1. Viviparous organisms vary greatly in their level of post-fertilization maternal provisioning and extensive provisioning (including very complex placentas) has evolved dozens of times in vertebrates. Through the use of species representing transitional states we aim to explore and develop empirically supported hypotheses that explain how such a complex trait has evolved. 2. In this study, we investigated the life histories and patterns of post-fertilization maternal provisioning in naturally occurring, all-female, hybrids between Poeciliopsis monacha, a viviparous species that produces large eggs and nourishes its embryos via stored yolk (lecithotrophy) and P.lucida, which produces small eggs and nourishes its embryos after fertilization via a follicular placenta (matrotrophy). Hybrids can be diploid or triploid, leading to different levels of gene dosage from the parental species. 3. We found that the extent of superfetation and average brood size of the hybrids did not differ significantly from their sexual parental species even though the latter was much lower in the hybrids. Moreover, the allodiploid, P. monacha-lucida, has intermediate sized eggs, whereas the allotriploid, P. monacha-monacha-lucida, produces eggs of similar size to those of P. monacha. The degree of post-fertilization maternal provisioning was unrelated to genomic dosages, with wild-caught hybrids being lecithotrophic, as seen in the maternal species (P. monacha). 4. Our results with naturally occurring P. monacha-lucida hybrids differed from those obtained with laboratory-synthesized hybrid clones, which were either lecithotrophic or weakly matrotrophic. Consequently, we propose two non-mutually exclusive hypotheses to explain why lecithotrophic clones might be favoured in the wild. One hypothesis suggests that lecithotrophic hybrids minimize competition with the matrotrophic paternal sexual species from which they require sperm to reproduce. Alternatively, we propose that natural selection has eliminated matrotrophic hybrids that suffer from intergenomic conflict in the degree of post-fertilization maternal provisioning. 5. We have thus identified an empirical system and developed testable hypotheses that will help elucidate the selective pressures that caused the evolution of post-fertilization maternal provisioning and potentially provide an opportunity to explore how epigenetic factors (e.g., intergenomic conflict) might influence this complex trait.
Journal Article